Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Ryanodine Receptor as Insecticide Target

Author(s): Arthur Samurkas, Li Yao, Hadiatullah Hadiatullah, Ruifang Ma, Yunxuan Xie, Rajamanikandan Sundarraj, Han Zuilhof and Zhiguang Yuchi*

Volume 28, Issue 1, 2022

Published on: 02 September, 2021

Page: [26 - 35] Pages: 10

DOI: 10.2174/1381612827666210902150224

Price: $65

Abstract

The ryanodine receptor (RyR) is one of the primary targets of commercial insecticides. The diamide insecticide family, including flubendiamide, chlorantraniliprole, cyantraniliprole, etc., targets insect RyRs and can be used to control a wide range of destructive agricultural pests. The diamide insecticides are highly selective against lepidopteran and coleopteran pests with relatively low toxicity for non-target species, such as mammals, fishes, and beneficial insects. However, recently mutations identified on insect RyRs have emerged and caused resistance in several major agricultural pests throughout different continents. This review paper summarizes the recent findings on the structure and function of insect RyRs as insecticide targets. Specifically, we examine the structures of RyRs from target and non-target species, which reveals the molecular basis for insecticide action and selectivity. We also examine the structural and functional changes of RyR caused by the resistance mutations. Finally, we examine the progress in RyR structure-based insecticide design and discuss how this might help the development of a new generation of green insecticides.

Keywords: Ryanodine receptor, insecticide, resistance, target, diamide, structural biology.

[1]
Smith JS, Imagawa T, Ma J, Fill M, Campbell KP, Coronado R. Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J Gen Physiol 1988; 92(1): 1-26.
[http://dx.doi.org/10.1085/jgp.92.1.1] [PMID: 2459298]
[2]
Pessah IN, Waterhouse AL, Casida JE. The calcium-ryanodine receptor complex of skeletal and cardiac muscle. Biochem Biophys Res Commun 1985; 128(1): 449-56.
[http://dx.doi.org/10.1016/0006-291X(85)91699-7] [PMID: 3985981]
[3]
Sattelle DB, Cordova D, Cheek TR. Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invert Neurosci 2008; 8(3): 107-19.
[http://dx.doi.org/10.1007/s10158-008-0076-4] [PMID: 18696132]
[4]
Yao R, Zhao DD, Zhang S, et al. Monitoring and mechanisms of insecticide resistance in Chilo suppressalis (Lepidoptera: Crambidae), with special reference to diamides. Pest Manag Sci 2017; 73(6): 1169-78.
[http://dx.doi.org/10.1002/ps.4439] [PMID: 27624654]
[5]
Ma J, Hayek SM, Bhat MB. Membrane topology and membrane retention of the ryanodine receptor calcium release channel. Cell Biochem Biophys 2004; 4-1(2): 207-24.
[http://dx.doi.org/10.1385/CBB:40:2:207]
[6]
Scott-Ward TS, Dunbar S J, Windass J D, Williams A J. Characterization of the ryanodine receptor-Ca2+ release channel from the thoracic tissues of the lepidopteran insect Heliothis virescens. J Membr Biol 2001; 179(2): 127-14-2.
[7]
Rosales RA, Fill M, Escobar AL. Calcium regulation of single ryanodine receptor channel gating analyzed using HMM/MCMC statistical methods. J Gen Physiol 2004; 123(5): 533-53.
[http://dx.doi.org/10.1085/jgp.200308868] [PMID: 15111644]
[8]
Du GG, MacLennan DH. Ca(2+) inactivation sites are located in the COOH-terminal quarter of recombinant rabbit skeletal muscle Ca(2+) release channels (ryanodine receptors). J Biol Chem 1999; 274(37): 26120-6.
[http://dx.doi.org/10.1074/jbc.274.37.26120] [PMID: 10473562]
[9]
Takeshima H, Nishimura S, Matsumoto T, et al. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 1989; 339(6224): 439-45.
[http://dx.doi.org/10.1038/339439a0] [PMID: 2725677]
[10]
Tanabe T, Beam KG, Adams BA, Niidome T, Numa S. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 1990; 346(6284): 567-9.
[http://dx.doi.org/10.1038/346567a0] [PMID: 2165570]
[11]
Nakai J, Imagawa T, Hakamat Y, Shigekawa M, Takeshima H, Numa S. Primary structure and functional expression from cDNA of the cardiac ryanodine receptor/calcium release channel. FEBS Lett 1990; 271(1-2): 169-77.
[http://dx.doi.org/10.1016/0014-5793(90)80399-4] [PMID: 2226801]
[12]
Nakai J, Sekiguchi N, Rando TA, Allen PD, Beam KG. Two regions of the ryanodine receptor involved in coupling with L-type Ca2+ channels. J Biol Chem 1998; 273(22): 13403-6.
[http://dx.doi.org/10.1074/jbc.273.22.13403] [PMID: 9593671]
[13]
Giannini G, Sorrentino V. Molecular structure and tissue distribution of ryanodine receptors calcium channels. Med Res Rev 1995; 15(4): 313-23.
[http://dx.doi.org/10.1002/med.2610150405] [PMID: 7475506]
[14]
Takeshima H, Nishi M, Iwabe N, et al. Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster. FEBS Lett 1994; 337(1): 81-7.
[http://dx.doi.org/10.1016/0014-5793(94)80634-9] [PMID: 8276118]
[15]
Xu X, Bhat MB, Nishi M, Takeshima H, Ma J. Molecular cloning of cDNA encoding a drosophila ryanodine receptor and functional studies of the carboxyl-terminal calcium release channel. Biophys J 2000; 78(3): 1270-81.
[http://dx.doi.org/10.1016/S0006-3495(00)76683-5] [PMID: 10692315]
[16]
Cordova D, Benner E, Sacher M, et al. Anthranilic diamides: A new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic Biochem Physiol 2006; 84: 196-214.
[http://dx.doi.org/10.1016/j.pestbp.2005.07.005]
[17]
Usherwood P, Vais HJ. Towards the development of ryanoid insecticides with low mammalian toxicity. 1995; 82: 247-54.
[http://dx.doi.org/10.1016/0378-4274(95)03558-3]
[18]
Tohnishi M, Nakao H, Furuya T, et al. Flubendiamide, a novel insecticide highly active against lepidopterous insect pests. Pestic Sci 2005; 30(4): 35-8-6-4.
[http://dx.doi.org/10.1584/jpestics.30.354]
[19]
Ebbinghaus-Kintscher U, Luemmen P, Lobitz N, et al. Phthalic acid diamides activate ryanodine-sensitive Ca2+ release channels in insects. Cell Calcium 2006; 39(1): 21-33.
[http://dx.doi.org/10.1016/j.ceca.2005.09.002] [PMID: 16219348]
[20]
Liu Y, Zhang Y, Liu S, et al. Distribution and degradation kinetics of cyhalodiamide in Chinese rice field environment. Chin J Chem Eng 2018; 26(10): 2185-91.
[http://dx.doi.org/10.1016/j.cjche.2018.07.003]
[21]
Lahm GP, Stevenson TM, Selby TP, et al. Rynaxypyr: A new insecticidal anthranilic diamide that acts as a potent and selective ryanodine receptor activator. Bioorg Med Chem Lett 2007; 17(22): 6274-9.
[http://dx.doi.org/10.1016/j.bmcl.2007.09.012] [PMID: 17884492]
[22]
Cordova D, Benner EA, Sacher MD, et al. Elucidation of the mode of action of Rynaxypyr®, a selective ryanodine receptor activator. In: Pesticide Chemistry. Crop Protection, Public Health, Environmental Safety 2007; pp. 121-6.
[http://dx.doi.org/10.1002/9783527611249.ch12]
[23]
Cordova D, Benner EA, Sacher MD, et al. The novel mode of action of anthranilic diamide insecticides: Ryanodine receptor activation. In: Synthesis and Chemistry of Agrochemicals VI. ACS Publications 2007; pp. 223-34.
[http://dx.doi.org/10.1021/bk-2007-0948.ch017]
[24]
Jeanguenat A. The story of a new insecticidal chemistry class: the diamides. Pest Manag Sci 2013; 69(1): 7-14.
[http://dx.doi.org/10.1002/ps.3406] [PMID: 23034936]
[25]
Selby TP, Lahm GP, Stevenson TM. A retrospective look at anthranilic diamide insecticides: discovery and lead optimization to chlorantraniliprole and cyantraniliprole. Pest Manag Sci 2017; 73(4): 658-65.
[http://dx.doi.org/10.1002/ps.4308] [PMID: 27146435]
[26]
Selby TP, Lahm GP, Stevenson TM, et al. Discovery of cyantraniliprole, a potent and selective anthranilic diamide ryanodine receptor activator with cross-spectrum insecticidal activity. Bioorg Med Chem Lett 2013; 23(23): 6341-5.
[http://dx.doi.org/10.1016/j.bmcl.2013.09.076] [PMID: 24135728]
[27]
Umetsu N, Shirai Y. Development of novel pesticides in the 21st century. J Pestic Sci 2020; 45(2): 54-74.
[http://dx.doi.org/10.1584/jpestics.D20-201] [PMID: 33132734]
[28]
Guo L, Lv H, Tan D, Liang N, Guo C, Chu D. Resistance to insecticides in the field and baseline susceptibility to cyclaniliprole of whitefly Bemisia tabaci (Gennadius) in China. Crop Prot 2020; 130: 105-265.
[http://dx.doi.org/10.1016/j.cropro.2019.105065]
[29]
Kousika J, Kuttalam S. Evaluation of tetraniliprole 200 sc against american serpentine leaf miner Liriomyza trifolii (Burgess) and its impact on natural enemies in Tomato. Pestic Res J 2020; 32(1): 165-71.
[http://dx.doi.org/10.5958/2249-524X.2020.00021.7]
[30]
Jeschke P. Status and outlook for acaricide and insecticide discovery. Pest Manag Sci 2021; 77(1): 64-76.
[http://dx.doi.org/10.1002/ps.6084] [PMID: 32926594]
[31]
Kambrekar D, Jahagirdar S, Aruna J. Tetraniliprole-new diamide insecticide molecule featuring novel mode of action against soybean insect pests. Biochem Cell Arch 2017; 17: 801-4.
[32]
Casida JE, Bryant RJ. The ABCs of pesticide toxicology: Amounts, biology, and chemistry. Toxicol Res (Camb) 2017; 6(6): 755-63.
[http://dx.doi.org/10.1039/c7tx00198c] [PMID: 30090540]
[33]
Qi S, Casida JE. Species differences in chlorantraniliprole and flubendiamide insecticide binding sites in the ryanodine receptor. Pestic Biochem Physiol 2013; 107(3): 321-6.
[http://dx.doi.org/10.1016/j.pestbp.2013.09.004] [PMID: 24267693]
[34]
Sarkar S, Dutta M, Roy S. Potential toxicity of flubendiamide in Drosophila melanogaster and associated structural alterations of its compound eye. Toxicol Environ Chem 2014; 96(7): 1075-87.
[http://dx.doi.org/10.1080/02772248.2014.997986]
[35]
Gnamm C, Jeanguenat A, Dutton AC, Grimm C, Kloer DP, Crossthwaite AJ. Novel diamide insecticides: sulfoximines, sulfonimidamides and other new sulfonimidoyl derivatives. Bioorg Med Chem Lett 2012; 22(11): 3800-6.
[http://dx.doi.org/10.1016/j.bmcl.2012.03.106] [PMID: 22552196]
[36]
Kato K, Kiyonaka S, Sawaguchi Y, et al. Molecular characterization of flubendiamide sensitivity in the lepidopterous ryanodine receptor Ca(2+) release channel. Biochemistry 2009; 48(43): 10342-52.
[http://dx.doi.org/10.1021/bi900866s] [PMID: 19807072]
[37]
Tao Y, Gutteridge S, Benner EA, et al. Identification of a critical region in the Drosophila ryanodine receptor that confers sensitivity to diamide insecticides. Insect Biochem Mol 2013; 43(9): 820-8.
[http://dx.doi.org/10.1016/j.ibmb.2013.06.006] [PMID: 23806522]
[38]
Ma R, Haji-Ghassemi O, Ma D, et al. Structural basis for diamide modulation of ryanodine receptor. Nat Chem Biol 2020; 16(11): 1246-54.
[http://dx.doi.org/10.1038/s41589-020-0627-5] [PMID: 32807966]
[39]
Troczka B, Zimmer CT, Elias J, et al. Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochem Mol Biol 2012; 42(11): 873-80.
[http://dx.doi.org/10.1016/j.ibmb.2012.09.001] [PMID: 22982600]
[40]
Richardson EB, Troczka BJ, Gutbrod O, Davies TE, Nauen R. Diamide resistance: 10 years of lessons from lepidopteran pests. J Pest Sci 2020; 93(3): 911-28.
[http://dx.doi.org/10.1007/s10340-020-01220-y]
[41]
Lv SL, Shi Y, Zhang JC, Liang P, Zhang L, Gao XW. Detection of ryanodine receptor target-site mutations in diamide insecticide-resistant Spodoptera frugiperda in China. Insect Sci 2021; 28(3): 639-48.
[http://dx.doi.org/10.1111/1744-7917.12896] [PMID: 33386702]
[42]
Talekar N, Shelton A. Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 1993; 38(1): 275-301.
[http://dx.doi.org/10.1146/annurev.en.38.010193.001423]
[43]
Steinbach D, Gutbrod O, Lümmen P, Matthiesen S, Schorn C, Nauen R. Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella. Insect Biochem Mol 2015; 63: 14-22.
[http://dx.doi.org/10.1016/j.ibmb.2015.05.001] [PMID: 25976541]
[44]
Wang X, Wu Y. High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. J Econ Entomol 2012; 105(3): 1019-23.
[http://dx.doi.org/10.1603/EC12059] [PMID: 22812143]
[45]
Ribeiro LM, Wanderley-Teixeira V, Ferreira HN, Teixeira ÁA, Siqueira HA. Fitness costs associated with field-evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bull Entomol Res 2014; 104(1): 88-96.
[http://dx.doi.org/10.1017/S0007485313000576] [PMID: 24229507]
[46]
Roditakis E, Steinbach D, Moritz G, et al. Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem Mol Biol 2017; 80: 11-20.
[http://dx.doi.org/10.1016/j.ibmb.2016.11.003] [PMID: 27845250]
[47]
Qin C, Wang C-H, Wang Y-Y, Sun S-Q, Wang H-H, Xue C-B. Resistance to diamide insecticides in Plutella xylostella (Lepidoptera: Plutellidae): comparison between lab-selected strains and field-collected populations. J Econ Entomol 2018; 111(2): 853-9.
[http://dx.doi.org/10.1093/jee/toy043] [PMID: 29529288]
[48]
Troczka BJ, Williams AJ, Williamson MS, Field LM, Lüemmen P, Davies TG. Stable expression and functional characterisation of the diamondback moth ryanodine receptor G4946E variant conferring resistance to diamide insecticides. Sci Rep 2015; 5(1): 14680.
[http://dx.doi.org/10.1038/srep14680] [PMID: 26424584]
[49]
Douris V, Papapostolou K-M, Ilias A, et al. Investigation of the contribution of RyR target-site mutations in diamide resistance by CRISPR/Cas9 genome modification in Drosophila. Insect Biochem Mol Biol 2017; 87: 127-35.
[http://dx.doi.org/10.1016/j.ibmb.2017.06.013] [PMID: 28669775]
[50]
Zuo Y, Wang H, Xu Y, et al. CRISPR/Cas9 mediated G4946E substitution in the ryanodine receptor of Spodoptera exigua confers high levels of resistance to diamide insecticides. Insect Biochem Mol Biol 2017; 89: 79-85.
[http://dx.doi.org/10.1016/j.ibmb.2017.09.005] [PMID: 28912111]
[51]
Guo L, Liang P, Zhou X, Gao X. Novel mutations and mutation combinations of ryanodine receptor in a chlorantraniliprole resistant population of Plutella xylostella (L.). Sci Rep 2014; 4: 6924.
[http://dx.doi.org/10.1038/srep06924] [PMID: 25377064]
[52]
Boaventura D, Bolzan A, Padovez FE, Okuma DM, Omoto C, Nauen R. Detection of a ryanodine receptor target-site mutation in diamide insecticide resistant fall armyworm, Spodoptera frugiperda. Pest Manag Sci 2020; 76(1): 47-54.
[http://dx.doi.org/10.1002/ps.5505] [PMID: 31157506]
[53]
Zuo YY, Ma HH, Lu WJ, et al. Identification of the ryanodine receptor mutation I4743M and its contribution to diamide insecticide resistance in Spodoptera exigua (Lepidoptera: Noctuidae). Insect Sci 2020; 27(4): 791-800.
[http://dx.doi.org/10.1111/1744-7917.12695] [PMID: 31140744]
[54]
Sun Y, Xu L, Chen Q, et al. Chlorantraniliprole resistance and its biochemical and new molecular target mechanisms in laboratory and field strains of Chilo suppressalis (Walker). Pest Manag Sci 2018; 74(6): 1416-23.
[http://dx.doi.org/10.1002/ps.4824] [PMID: 29235708]
[55]
Huang JM, Rao C, Wang S, et al. Multiple target-site mutations occurring in lepidopterans confer resistance to diamide insecticides. Insect Biochem Mol Biol 2020; 121: 103367.
[http://dx.doi.org/10.1016/j.ibmb.2020.103367] [PMID: 32243905]
[56]
Gong C, Yao X, Yang Q, et al. Fitness Costs of Chlorantraniliprole Resistance Related to the SeNPF Overexpression in the Spodoptera exigua (Lepidoptera: Noctuidae). Int J Mol Sci 2021; 22(9): 5027.
[http://dx.doi.org/10.3390/ijms22095027] [PMID: 34068540]
[57]
Lin L, Liu C, Qin J, et al. Crystal structure of ryanodine receptor N-terminal domain from Plutella xylostella reveals two potential species-specific insecticide-targeting sites. Insect Biochem Mol Biol 2018; 92: 73-83.
[http://dx.doi.org/10.1016/j.ibmb.2017.11.009] [PMID: 29191465]
[58]
Zhou Y, Wang W, Salauddin NM, et al. Crystal structure of the N-terminal domain of ryanodine receptor from the honeybee, Apis mellifera. Insect Biochem Mol Biol 2020; 125: 103454.
[http://dx.doi.org/10.1016/j.ibmb.2020.103454] [PMID: 32781205]
[59]
Zhou Y, Ma D, Lin L, You M, Yuchi Z, You S. Crystal structure of the ryanodine receptor SPRY2 domain from the diamondback moth provides insights into the development of novel insecticides. J Agric Food Chem 2020; 68(6): 1731-40.
[http://dx.doi.org/10.1021/acs.jafc.9b08151] [PMID: 31951399]
[60]
Xu T, Yuchi Z. Crystal structure of diamondback moth ryanodine receptor Repeat34 domain reveals insect-specific phosphorylation sites. BMC Biol 2019; 17(1): 77.
[http://dx.doi.org/10.1186/s12915-019-0698-5] [PMID: 31597572]
[61]
Samurkas A, Fan X, Ma D, et al. Discovery of potential species-specific green insecticides targeting the lepidopteran ryanodine receptor. J Agric Food Chem 2020; 68(15): 4528-37.
[http://dx.doi.org/10.1021/acs.jafc.0c01063] [PMID: 32207934]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy