Ryanodine Receptors for Drugs and Insecticides: An Overview

Author(s): Zhiqiang Sun, Hui Xu*.

Journal Name: Mini-Reviews in Medicinal Chemistry

Volume 19 , Issue 1 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Ryanodine receptors (RyRs) are calcium channels located on the endo(sarco)plasmic reticulum of muscle cells and neurons. They regulate the release of stored intracellular calcium and play a critical role in muscle contraction. The N-terminal part of these receptors accounts for roughly 80% and contains the binding sites for diverse RyRs modulators. The C-terminal domain contains the transmembrane region. This review summarizes the current knowledge about the molecular biology of insect RyRs, chemicals targeting mammal or insect RyRs, and the reasons for mammal RyR-related diseases and diamides resistances. It may lay the foundation for effective management of mammal RyR-related diseases and diamides resistances.

Keywords: Ryanodine, ryanodine receptors, mammal RyR-related diseases, diamides insecticides, insecticide resistant, MicroRNA.

[1]
Sattell, D.B.; Cordova, D.; Cheek, T.R. Insect ryanodine receptors: molecular targets for novel pest control chemicals. Invert. Neurosci., 2008, 8, 107-119.
[2]
Amador, F.J.; Stathopulos, P.B.; Enomoto, M.; Ikura, M. Ryanodine receptor calcium release channels: Lessons from structure-function studies. FEBS J., 2013, 280, 5456-5470.
[3]
Lanner, J.T.; Georgiou, D.K.; Joshi, A.D.; Hamilton, S.L. Ryanodine receptors: Structure, expression, molecular details, and function in calcium release. CSH. Perspect. Biol, 2010, 2, a003996.
[4]
Jefferies, P.R.; Blumenkopf, T.A.; Gengo, P.J.; Cole, L.C.; Casida, J.E. Ryanodine action at calcium release channels. 1. importance of hydroxyl substituents. J. Med. Chem., 1996, 39, 2331-2338.
[5]
Lahm, G.P.; Cordova, D.; Barry, J.D. New and selective ryanodine receptor activators for insect control. Bioorg. Med. Chem., 2009, 17, 4127-4133.
[6]
Schwarz, T.; Snow, T.A.; Santee, C.; Mulligan, C.C.; Class, T.J.; Wadsley, M.; Nanita, S.C. QuEChERS multiresidue method validation and mass spectrometric assessment for the novel anthranilic diamide insecticides chlorantraniliprole and cyantraniliprole. J. Agric. Food Chem., 2011, 59, 814-821.
[7]
Clark, D.A.; Lahm, G.P.; Smith, B.K.; Barry, J.D.; Clagg, D.G. Synthesis of insecticidal fluorinated anthranilic diamides. Bioorg. Med. Chem., 2008, 16, 3163-3170.
[8]
Troczka, B.J.; Williamson, M.S.; Field, L.M.; Davies, T.G.E. Rapid selection for resistance to diamide insecticides in Plutella xylostella via specific amino acid polymorphisms in the ryanodine receptor. Neurotoxicology, 2017, 60, 224-233.
[9]
Troczka, B.J.; Zimmer, C.T.; Elias, J.; Schorn, C.; Bass, C.; Davies, T.G.; Field, L.M.; Williamson, S.M.; Slater, R.; Nauen, R. 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, 873-880.
[10]
Feng, M.L.; Li, Y.; Zhu, H.; Zhao, L.; Xi, B.B.; Ni, J. Synthesis, insecticidal activity, and structure-activity relationship of trifluoromethyl-containing phthalic acid diamide structures. J. Agric. Food Chem., 2010, 58, 10999-11006.
[11]
Gaburjakova, M.; Bal, N.C.; Gaburjakova, J.; Periasamy, M. Functional interaction between calsequestrin and ryanodine receptor in the heart. Cell. Mol. Life Sci., 2012, 70, 2935-2945.
[12]
Feng, Q.; Liu, Z.L.; Xiong, L.; Wang, M.; Li, Y.; Li, Z. Synthesis and insecticidal activities of novel anthranilic diamides containing modified N-pyridylpyrazoles. J. Agric. Food Chem., 2010, 58, 12327-12336.
[13]
Zhang, J.; Xu, J.; Wang, B.; Li, Y.; Xiong, L.X.; Li, Y.; Xiong, L.; Li, Y.; Ma, Y.; Li, Z. Synthesis and insecticidal activities of novel anthranilic diamides containing acylthiourea and acylurea. J. Agric. Food Chem., 2012, 60, 7565-7572.
[14]
Kaufmann, A.; Kraft, B.; Michaleksauberer, A.; Weigl, L. Novel ryanodine receptor mutation that may cause malignant hyperthermia. Anesthesiology, 2008, 109, 457-464.
[15]
Xin, W.; Soder, R.P.; Cheng, Q.; Rovner, E.S.; Petkov, G.V. Selective inhibition of phosphodiesterase 1 relaxes urinary bladder smooth muscle: role for ryanodine receptor-mediated BK channel activation. Am. J. Physiol. Cell Physiol., 2012, 303, 1079-1089.
[16]
Choia, R.H.; Koeniga, X.; Launikonis, B.A. Dantrolene requires Mg2+ to arrest malignant hyperthermia. Proc. Natl. Acad. Sci. USA, 2017, 114, 4576-4578.
[17]
Lunde, P.K.; Sejersted, O.M. Ryanodine binding sites measured in small skeletal muscle biopsies. Scand. J. Clin. Lab. Invest., 1997, 57, 569-580.
[18]
Cui, L.; Rui, C.; Yang, D.; Wang, Z.; Yuan, H. De novo transcriptome and expression profile analyses of the Asian corn borer (Ostrinia furnacalis) reveals relevant flubendiamide response genes. BMC Genomics, 2017, 18, 20.
[19]
Zhu, B.; Li, X.; Liu, Y.; Gao, X.; Liang, P. Global identification of microRNAs associated with chlorantraniliprole resistance in diamondback moth Plutella xylostella (L.). Sci. Rep., 2017, 7, 40713.
[20]
Li, X.; Guo, L.; Zhou, X.; Gao, X.; Liang, P. miRNAs regulated overexpression of ryanodine receptor is involved in chlorantraniliprole resistance in Plutella xylostella (L.). Sci. Rep., 2015, 5, 14095.
[21]
Zhu, B.; Xu, M.; Shi, H.; Gao, X.; Liang, P. Genome-wide identification of lncRNAs associated with chlorantraniliprole resistance in diamondback moth Plutella xylostella (L.). BMC Genomics, 2017, 18, 380.
[22]
Zalk, R.; Lehnart, S.E.; Marks, A.R. Modulation of the ryanodine receptor and intracellular calcium. Annu. Rev. Biochem., 2007, 76, 367-385.
[23]
Masuda, K.; Koshimizu, M.; Nagatomo, M.; Inoue, M. Asymmetric total synthesis of (+)-ryanodol and (+)-ryanodine. Chem. Eur. J., 2016, 22, 230-236.
[24]
Kato, K.; Kiyonaka, S.; Sawaguchi, Y.; Tohnishi, M.; Masaki, T.; Yasokawa, N.; Mizuno, Y.; Mori, E.; Inoue, K.; Hamachi, I.; Takeshima, H.; Mori, Y. Molecular characterization of flubendiamide sensitivity in the lepidopterous ryanodine receptor Ca2+ release channel. Biochemistry, 2009, 48, 10342-10352.
[25]
Butandaochoa, A.; Hojer, G.; Moralestlalpan, V.; Diazmunoz, M. Recognition and activation of ryanodine receptors by purines. Curr. Med. Chem., 2006, 13, 647-657.
[26]
Roditakis, E.; Steinbach, D.; Moritz, G.; Vasakis, E.; Stavrakaki, M.; Ilias, A.; García-Vidal, L.; Martínez-Aguirre, M.D.; Bielza, P.; Morou, E.; Silva, J.E.; Silva, W.M.; Siqueira, H.A.; Iqbal, S.; Troczka, B.J.; Williamson, M.S.; Bass, C.; Tsagkarakou, A.; Vontas, J.; Nauen, R. Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta. Insect Biochem. Mol. Biol., 2016, 80, 11-20.
[27]
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.
[28]
Yan, H.; Xue, C.; Li, G.; Zhao, X.; Che, X.; Wang, L. Flubendiamide resistance and Bi-PASA detection of ryanodine receptor G4946E mutation in the diamondback moth (Plutella xylostella L.). Pestic. Biochem. Physiol., 2014, 115, 73-77.
[29]
Fill, M.; Copello, J.A. Ryanodine receptor calcium release channels. Physiol. Rev., 2002, 82, 893-922.
[30]
Leeb, T.; Brenig, B. Ryanodine receptors and their role in genetic diseases. Int. J. Mol. Med., 1998, 2, 293-593.
[31]
Guerrerohernandez, A.; Avila, G.R.; Rueda, A. Ryanodine receptors as leak channels. Eur. J. Pharmacol., 2014, 739, 26-38.
[32]
Scoote, M.; Williams, A.J. The cardiac ryanodine receptor (calcium release channel): Emerging role in heart failure and arrhythmia pathogenesis. Cardiovasc. Res., 2002, 56, 359-372.
[33]
Yan, Z.; Bai, X.; Yan, C.; Wu, J.; Li, Z.; Xie, T.; Peng, W.; Yin, C.; Li, X.; Scheres, S.H.W.; Shi, Y.; Yan, N. Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature, 2015, 517, 50-55.
[34]
Bai, X.; Yan, Z.; Wu, J.; Li, Z.; Yan, N. The central domain of RyR1 is the transducer for long-range allosteric gating of channel opening. Cell Res., 2016, 26, 995-1006.
[35]
Peng, W.; Shen, H.; Wu, J.; Guo, W.; Pan, X.; Wang, R.; Chen, S.R.W.; Yan, N. Structural basis for the gating mechanism of the type 2 ryanodine receptor RyR2. Science, 2016, 26, 995-1006.
[36]
Wan, P.; Guo, W.; Yang, Y.; Lu, F.; Lu, W.; Li, G. RNAi suppression of the ryanodine receptor gene results in decreased susceptibility to chlorantraniliprole in Colorado potato beetle Leptinotarsa decemlineata. J. Insect Physiol., 2014, 63, 48-55.
[37]
Liu, G.; Ju, X.; Cheng, J.; Liu, Z. 3D-QSAR studies of insecticidal anthranilic diamides as ryanodine receptor activators using CoMFA, CoMSIA and DISCOtech. Chemosphere, 2010, 78, 300-306.
[38]
Huang, L.; Lu, M.; Han, G.; Du, Y.; Wang, J. Sublethal effects of chlorantraniliprole on development, reproduction and vitellogenin gene (CsVg) expression in the rice stem borer, Chilo suppressalis. Pest Manag. Sci., 2016, 72, 2280-2286.
[39]
Guo, L.; Tang, B.; Dong, W.; Liang, P.; Gao, X. Cloning, characterisation and expression profiling of the cDNA encoding the ryanodine receptor in diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Pest Manag. Sci., 2012, 68, 1605-1614.
[40]
Mackrill, J.J. Ryanodine receptor calcium channels and their partners as drug targets. Biochem. Pharmacol., 2010, 79, 1535-1543.
[41]
Prestle, J.; Quinn, F.R.; Smith, G.L. Ca2+ handling proteins and heart failure: Novel molecular targets? Curr. Med. Chem., 2003, 10, 967-981.
[42]
Wehrens, X.H.; Lehnart, S.E.; Reiken, S.; Vest, J.A.; Wronska, A.; Marks, A.R. Ryanodine receptor/calcium release channel PKA phosphorylation: A critical mediator of heart failure progression. Proc. Natl. Acad. Sci. USA, 2006, 103, 511-518.
[43]
Selby, T.P.; Lahm, G.P.; Stevenson, T.M.; Hughes, K.A.; Cordova, D.; Annan, I.B.; Barry, J.D.; Benner, E.A.; Currie, M.J.; Pahutski, T.F. Discovery of cyantraniliprole, a potent and selective anthranilic diamide ryanodine receptor activator with cross-spectrum insecticidal activity. Bioorg. Med. Chem. Lett., 2013, 23, 6341-6345.
[44]
Sun, L.; Zhang, H.J.; Quan, L.; Yan, W.T.; Yue, Q.; Li, Y.; Qiu, G. Characterization of the ryanodine receptor gene with a unique 3′-UTR and alternative splice site from the oriental fruit moth. J. Insect Sci., 2016, 16, 1-9.
[45]
Wang, K.; Jiang, X.; Yuan, G.; Shang, F.; Wang, J. Molecular characterization, mRNA expression and alternative splicing of ryanodine receptor gene in the brown citrus aphid, Toxoptera citricida (Kirkaldy). Int. J. Mol. Sci., 2015, 16, 15220-15234.
[46]
Takeshima, H.; Nishi, M.; Iwabe, N.; Miyata, T.; Hosoya, T.; Masai, I.; Hotta, Y. Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster. FEBS Lett., 1994, 337, 81-87.
[47]
Puente, E.; Suner, M.; Evans, A.D.; Mccaffery, A.R.; Windass, J.D. Identification of a polymorphic ryanodine receptor gene from Heliothis virescens (Lepidoptera: noctuidae). Insect Biochem. Mol. Biol., 2000, 30, 335-347.
[48]
Schmitt, M.; Turberg, A.; Londershausen, M.; Dorn, A. Binding sites for Ca2+-channel effectors and ryanodine in Periplaneta americana-possible targets for new insecticides. Pestic. Sci., 1996, 48, 375-388.
[49]
Collet, C. Excitation-contraction coupling in skeletal muscle fibers from adult domestic honeybee. Pflügers Archiv-. Eur. J. Phys., 2009, 458, 601-612.
[50]
Arnon, A.; Cook, B.; Montell, C.; Selinger, Z.; Minke, B. Calmodulin regulation of calcium stores in phototransduction of Drosophila. Science, 1997, 275, 1119-1121.
[51]
Troczka, B.J.; Williams, A.J.; Williamson, M.S.; Field, L.M.; Lüemmen, P.; Davies, T.G.E. Stable expression and functional characterisation of the diamondback moth ryanodine receptor G4946E variant conferring resistance to diamide insecticides. Sci. Rep., 2015, 5, 14680.
[52]
Xu, C.; Han, A.; Virgil, S.C.; Reisman, S.E. Chemical synthesis of (+)-ryanodine and (+)-20-deoxyspiganthine. ACS Cent. Sci., 2017, 3, 278-282.
[53]
Ledbetter, M.W.; Preiner, J.; Louis, C.F.; Mickelson, J.R. Tissue distribution of ryanodine receptor isoforms and alleles determined by reverse transcription polymerase chain reaction. J. Biol. Chem., 1994, 269, 31544-31551.
[54]
Liu, J.; Li, Y.; Zhang, X.; Hua, X.; Wu, C.; Wei, W.; Wan, Y.; Cheng, D.; Xiong, L.; Yang, N.; Song, H.; Li, Z. Novel anthranilic diamide scaffolds containing N-substituted phenylpyrazole as potential ryanodine Receptor activators. J. Agric. Food Chem., 2016, 64, 3697-3704.
[55]
Qi, S.; Lummen, P.; Nauen, R.; Casida, J.E. Diamide insecticide target site specificity in the Heliothis and Musca ryanodine receptors relative to toxicity. J. Agric. Food Chem., 2014, 62, 4077-4082.
[56]
Buck, E.; Zimanyi, I.; Abramson, J.J.; Pessah, I.N. Ryanodine stabilizes multiple conformational states of the skeletal muscle calcium release channel. J. Biol. Chem., 1992, 267, 23560-23567.
[57]
Chen, S.R.; Li, X.; Ebisawa, K.; Zhang, L. Functional characterization of the recombinant type 3 Ca2+ release channel (ryanodine receptor) expressed in HEK293 cells. J. Biol. Chem., 1992, 272, 24234-24246.
[58]
Donoso, P.; Prieto, H.; Hidalgo, C. Luminal calcium regulates calcium release in triads isolated from frog and rabbit skeletal muscle. Biophys. J., 1995, 68, 507-515.
[59]
Waterhouse, A.L.; Pessah, I.N.; Francini, A.O.; Casida, J.E. Structural aspects of ryanodine action and selectivity. J. Med. Chem., 1987, 30, 710-716.
[60]
Chuang, K.V.; Xu, C.K.; Reisman, S.E. A 15-step synthesis of (+)-ryanodol. Science, 2016, 353, 912-915.
[61]
Nagatomo, M.; Koshimizu, M.; Masuda, K.; Tabuchi, T.; Urabe, D.; Inoue, M. Total synthesis of ryanodol. J. Am. Chem. Soc., 2014, 136, 5916-5919.
[62]
Pepper, B.P.; Carruth, L.A. A new plant insecticide for control of the european corn borer. J. Econ. Entomol., 1945, 38, 59-66.
[63]
Bannister, R.A. Dantrolene-induced inhibition of skeletal L-type Ca2+ current requires RyR1 expression. BioMed Res. Int., 2013, 2013, 390493.
[64]
Zhao, X.; Weisleder, N.; Han, X.; Pan, Z.; Parness, J.; Brotto, M.; Ma, J. Azumolene inhibits a component of store-operated calcium entry coupled to the skeletal muscle ryanodine receptor. J. Biol. Chem., 2006, 281, 33477-33486.
[65]
Durham, W.J.; Aracena-parks, P.; Long, C.; Rossi, A.E.; Goonasekera, S.A.; Boncompagni, S.; Galvan, D.L.; Gilman, C.P.; Baker, M.R.; Shirokova, N.; Protasi, F.; Dirksen, R.T.; Hamilton, S.L. RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1 knockin mice. Cell, 2008, 133, 53-65.
[66]
Lanner, J.T.; Georgiou, D.K.; Dagnino-Acosta, A.; Ainbinder, A.; Cheng, Q.; Joshi, A.D.; Chen, Z.; Yarotskyy, V.; Oakes, J.; Lee, C.S.; Monroe, T.O.; Santillan, A.; Dong, K.; Goodyear, L.J.; Ismailov, I.I. Rodney, G.G.; Dirksen, R.T.; Hamilton, S.L. AICAR prevents heat induced sudden death in RyR1 mutant mice independent of AMPK activation. Nat. Med., 2012, 18, 244-251.
[67]
Pessah, I.N.; Lehmler, H.J.; Robertson, L.W.; Perez, C.F.; Cabrales, E.; Bose, D.D.; Feng, W. Enantiomeric specificity of (-)-2,2′,3,3′,6,6′-hexachlorobiphenyl toward ryanodine receptor types 1 and 2. Chem. Res. Toxicol., 2009, 22, 201-207.
[68]
Kim, K.H.; Inan, S.Y.; Berman, R.F.; Pessah, I.N. Excitatory and inhibitory synaptic transmission is differentially influenced by two ortho-substituted polychlorinated biphenyls in the hippocampal slice preparation. Toxicol. Appl. Pharmacol., 2009, 237, 168-177.
[69]
Fusi, F.; Iozzi, D.; Sgaragli, G.; Frosini, M. 3,5-di-t-butylcatechol (DTCAT) as an activator of rat skeletal muscle ryanodine receptor Ca2+ channel (RyRC). Biochem. Pharmacol., 2005, 69, 485-491.
[70]
Herrmannfrank, A.; Richter, M.; Sarkozi, S.; Mohr, U.; Lehmannhorn, F. 4-Chloro-m-cresol, a potent and specific activator of the skeletal muscle ryanodine receptor. BBA-Gen. Subjects, 1996, 1289, 31-40.
[71]
Eguchi, K.; Kato, H.; Fujiwara, Y.; Losung, F.; Mangindaan, R.E.; De Voogd, N.J.; Takeya, M.; Tsukamoto, S. Bastadins, brominated-tyrosine derivatives, suppress accumulation of cholesterol ester in macrophages. Bioorg. Med. Chem. Lett., 2015, 25, 5389-5392.
[72]
Aoki, S.; Cho, S.; Hiramatsu, A.; Kotoku, N.; Kobayashi, M. Bastadins, cyclic tetramers of brominated-tyrosine derivatives, selectively inhibit the proliferation of endothelial cells. J. Nat. Med., 2006, 60, 231-235.
[73]
Zieminska, E.; Lazarewicz, J.W.; Couladouros, E.A.; Moutsos, V.I.; Pitsinos, E.N. Open-chain half-bastadins mimic the effects of cyclic bastadins on calcium homeostasis in cultured neurons. Bioorg. Med. Chem. Lett., 2008, 18, 5734-5737.
[74]
Masuno, M.N.; Pessah, I.N.; Olmstead, M.M.; Molinski, T.F. Simplified cyclic analogues of bastadin-5. Structure-activity relationships for modulation of the RyR1/FKBP12 Ca2+ channel complex. J. Med. Chem., 2006, 49, 4497-4511.
[75]
Kaftan, E.J.; Marks, A.R.; Ehrlich, B.E. Effects of rapamycin on ryanodine receptor/Ca2+-release channels from cardiac muscle. Circ. Res., 1996, 78, 990-997.
[76]
Dammermann, W.; Zhang, B.; Nebel, M.; Cordiglieri, C.; Odoardi, F.; Kirchberger, T.; Kawakami, N.; Dowden, J.; Schmid, F.; Dornmair, K.; Hohenegger, M.; Flugel, A.; Guse, A.H.; Potter, B.V. NAADP-mediated Ca2+ signaling via type 1 ryanodine receptor in T cells revealed by a synthetic NAADP antagonist. Proc. Natl. Acad. Sci. USA, 2009, 106, 10678-10683.
[77]
Papineni, R.V.; Oconnell, K.M.; Zhang, H.; Dirksen, R.T.; Hamilton, S.L. Suramin interacts with the calmodulin binding site on the ryanodine receptor, RYR1. J. Biol. Chem., 2002, 277, 49167-49174.
[78]
Sun, J.; Yamaguchi, N.; Xu, L.; Eu, J.P.; Stamler, J.S.; Meissner, G. Regulation of the cardiac muscle ryanodine receptor by O2 tension and S-nitrosoglutathione. Biochemistry, 2008, 47, 13985-13990.
[79]
Xu, L.; Eu, J.P.; Meissner, G.; Stamler, J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science, 1998, 279, 234-237.
[80]
Zherebitskaya, E.; Schapansky, J.; Akude, E.; Smith, D.R.; Van der Ploeg, R.; Solovyova, N.; Verkhratsky, A.; Fernyhough, P. Sensory neurons derived from diabetic rats have diminished internal Ca2+ stores linked to impaired re-uptake by the endoplasmic reticulum. ASN Neuro, 2012, 4, e00072.
[81]
Mochizuki, M.; Yano, M.; Oda, T.; Tateishi, H.; Kobayashi, S.; Yamamoto, T.; Ikeda, Y.; Ohkusa, T.; Ikemoto, N.; Matsuzaki, M. Scavenging free radicals by low-dose carvedilol prevents redox-dependent Ca2+ leak via stabilization of ryanodine receptor in heart failure. J. Am. Coll. Cardiol., 2007, 49, 1722-1732.
[82]
Watanabe, H.; Chopra, N.; Laver, D.R.; Hwang, H.S.; Davies, S.S.; Roach, D.E.; Duff, H.J.; Roden, D.M.; Wilde, A.A.; Knollmann, B.C. Flecainide prevents catecholaminergic polymorphic ventricular tachycardia in mice and humans. Nat. Med., 2009, 15, 380-383.
[83]
Mehra, D.; Imtiaz, M.S.; Van Helden, D.F.; Knollmann, B.C.; Laver, D.R. Multiple modes of ryanodine receptor 2 inhibition by flecainide. Mol. Pharmacol., 2014, 86, 696-706.
[84]
Jiang, X.; Liu, W.; Deng, J.; Lan, L.; Xue, X.; Zhang, C.; Ikeda, Y.; Ohkusa, T.; Ikemoto, N.; Matsuzaki, M. Polydatin protects cardiac function against burn injury by inhibiting sarcoplasmic reticulum Ca2+ leak by reducing oxidative modification of ryanodine receptors. Free Radic. Biol. Med., 2013, 60, 292-299.
[85]
Fritsch, E.B.; Connon, R.E.; Werner, I.; Davies, R.E.; Beggel, S.; Feng, W.; Pessah, I.N. Triclosan impairs swimming behavior and alters expression of excitation-contraction coupling proteins in fathead minnow (Pimephales promelas). Environ. Sci. Technol., 2013, 47, 2008-2017.
[86]
Murayama, T.; Ogawa, Y. Characterization of type 3 ryanodine receptor (RyR3) of sarcoplasmic reticulum from rabbit skeletal muscles. J. Biol. Chem., 1997, 272, 24030-24037.
[87]
Shiomi, K.; Matsui, R.; Kakei, A.; Yamaguchi, Y.; Masuma, R.; Hatano, H.; Arai, N.; Isozaki, M.; Tanaka, H.; Kobayashi, S.; Turberg, A.; Omura, S. Verticilide, a new ryanodine-binding inhibitor, produced by Verticillium sp. FKI-1033. J. Antibiot., 2010, 63, 77-82.
[88]
Ni, J.; Auston, D.A.; Freilich, D.; Muralidharan, S.; Sobie, E.A.; Kao, J.P. Photochemical gating of intracellular Ca2+ release channels. J. Am. Chem. Soc., 2007, 129, 5316-5317.
[89]
Guerreiro, S.; Toulorge, D.; Hirsch, E.C.; Marien, M.; Sokoloff, P.; Michel, P.P. Paraxanthine, the primary metabolite of caffeine, provides protection against dopaminergic cell death via stimulation of ryanodine receptor channels. Mol. Pharmacol., 2008, 74, 980-989.
[90]
Jin, S.W.; Choi, C.Y.; Hwang, Y.P.; Kim, H.G.; Kim, S.J.; Chung, Y.C.; Lee, K.J.; Jeong, T.C.; Jeong, H.G. Betulinic acid Increases eNOS phosphorylation and NO synthesis via the calcium-signaling pathway. J. Agric. Food Chem., 2016, 64, 785-791.
[91]
Lehmberg, E.; Casida, J.E. Similarity of insect and mammalian ryanodine binding sites. Pestic. Biochem. Physiol., 1994, 48, 145-152.
[92]
Steinbach, D.; Gutbrod, O.; Lummen, 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. Biol., 2015, 63, 14-22.
[93]
Wang, X.; Khakame, S.K.; Ye, C.; Yang, Y.; Wu, Y. Characterisation of field-evolved resistance to chlorantraniliprole in the diamondback moth, Plutella xylostella, from China. Pest Manag. Sci., 2013, 69, 661-665.
[94]
Nauen, R.; Steinbach, D. Resistance to Diamide Insecticides in Lepidopteran Pests.In: Advances in Insect Control and Resistance Management; Horowitz, A.R.; Ishaaya, I., Eds.; Springer International Publishing: Switzerland, 2016, pp. 219-240.
[95]
Cordova, D.; Benner, E.A.; Sacher, M.D.; Rauh, J.J.; Sopa, J.S.; Lahm, G.P.; Selby, T.P.; Stevenson, T.M.; Flexner, L.; Gutteridge, S.; Rhoades, D.F.; Wu, L.; Smith, R.M.; Tao, Y. Anthranilic diamides: A new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic. Biochem. Physiol., 2006, 84, 196-214.
[96]
Nauen, R. Insecticide mode of action: Return of the ryanodine receptor. Pest Manag. Sci., 2006, 62, 690-692.
[97]
Vega, A.V.; Ramosmondragon, R.; Calderonrivera, A.; Zarainherzberg, A.; Avila, G. Calcitonin gene-related peptide restores disrupted excitation-contraction coupling in myotubes expressing central core disease mutations in RyR1. J. Physiol., 2011, 589, 4649-4669.
[98]
Priori, S.G.; Napolitano, C.; Memmi, M.; Colombi, B.; Drago, F.; Gasparini, M.; Delogu, A.B. Clinical and molecular characterization of patients with catecholaminergic polymorphic ventricular tachycardia. Circulation, 2002, 106, 69-74.
[99]
Priori, S.G.; Napolitano, C.; Tiso, N.; Memmi, M.; Vignati, G.; Bloise, R.; Sorrentino, V.; Danieli, G.A. Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia. Circulation, 2001, 103, 196-200.
[100]
Ying, S.; Chang, D.C.; Lin, S. The MicroRNA (miRNA): Overview of the RNA genes that modulate gene function. Mol. Biotechnol., 2008, 38, 257-268.
[101]
Beavers, D.L.; Wang, W.; Ather, S.; Voigt, N.; Garbino, A.; Dixit, S.S.; Landstrom, A.P.; Li, N. \Wang, Q.; Olivotto, I.; Dobrev, D.; Ackerman, M.J.; Wehrens, X.H. Mutation E169K in junctophilin-2 causes atrial fibrillation due to impaired RyR2 stabilization. J. Am. Coll. Cardiol., 2013, 62, 2010-2019.
[102]
Chiang, D.Y.; Kongchan, N.; Beavers, D.L.; Alsina, K.M.; Voigt, N.; Neilson, J.R.; Jakob, H.; Martin, J.F.; Dobrev, D.; Wehrens, X.H.; Li, N. Loss of microRNA-106b-25 cluster promotes atrial fibrillation by enhancing ryanodine receptor type-2 expression and calcium release. Circ-arrhythmia Elec., 2014, 7, 1214-1222.
[103]
Belevych, A.E.; Sansom, S.E.; Terentyeva, R.; Ho, H.; Nishijima, Y.; Martin, M.M.; Jindal, H.K.; Rochira, J.A.; Kunitomo, Y.; Abdellatif, M.; Carnes, C.A.; Elton, T.S.; Gyorke, S.; Terentyev, D. MicroRNA-1 and -133 increase arrhythmogenesis in heart failure by dissociating phosphatase activity from RyR2 complex. PLoS One, 2011, 6, e28324.
[104]
Zhang, L.; Liu, Y.; Song, F.; Zheng, H.; Hu, L.; Lu, H.; Liu, P.; Hao, X.; Zhang, W.; Chen, K. Functional SNP in the microRNA-367 binding site in the 3′UTR of the calcium channel ryanodine receptor gene 3 (RYR3) affects breast cancer risk and calcification. Proc. Natl. Acad. Sci. USA, 2011, 108, 13653-13658.
[105]
Tao, Y.; Gutteridge, S.; Benner, E.A.; Wu, L.; Rhoades, D.F.; Sacher, M.D.; Cordova, D. Identification of a critical region in the Drosophila ryanodine receptor that confers sensitivity to diamide insecticides. Insect Biochem. Mol. Biol., 2013, 43, 820-828.
[106]
Ebbinghaus-Kintscher, U.; Luemmen, P.; Lobitz, N.; Schulte, T.; Funke, C.; Fischer, R.; Masaki, T.; Yasokawa, N.; Tohnishi, M. Phthalic acid diamides activate ryanodine-sensitive Ca2+ release channels in insects. Cell Cal., 2006, 39, 21-33.
[107]
Gong, W.; Yan, H.; Gao, L.; Guo, Y.; Xue, C. Chlorantraniliprole resistance in the diamondback moth (Lepidoptera: Plutellidae). J. Econ. Entomol., 2014, 107, 806-814.
[108]
Ramachandran, S.; Chakraborty, A.; Xu, L.; Mei, Y.; Samso, M.; Dokholyan, N.V.; Meissner, G. Structural determinants of skeletal muscle ryanodine receptor gating. J. Biol. Chem., 2013, 288, 6154-6165.
[109]
Fessenden, J.D.; Chen, L.; Wang, Y.; Paolini, C.; Franziniarmstrong, C.; Allen, P.D.; Pessah, I.N. Ryanodine receptor point mutant E4032A reveals an allosteric interaction with ryanodine. Proc. Natl. Acad. Sci. USA, 2001, 98, 2865-2870.
[110]
Douris, V.; Papapostolou, K.M.; Ilias, A.; Roditakis, E.; Kounadi, S.; Riga, M.; Nauen, R.; Vontas, J. 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, 127-135.
[111]
Zimmer, C.T.; Garrood, W.T.; Puinean, A.M.; Eckelzimmer, M.; Williamson, M.S.; Davies, T.G.; Bass, C.A. CRISPR/Cas9 mediated point mutation in the alpha 6 subunit of the nicotinic acetylcholine receptor confers resistance to spinosad in Drosophila melanogaster. Insect Biochem. Mol. Biol., 2016, 73, 62-69.
[112]
Sang, S.; Shu, B.; Yi, X.; Liu, J.; Hu, M.; Zhong, G. Cross-resistance and baseline susceptibility of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) to cyantraniliprole in the south of China. Pest Manag. Sci., 2015, 72, 922-928.
[113]
Lin, Q.; Jin, F.; Hu, Z.; Chen, H.; Yin, F.; Li, Z.; Dong, X.; Zhang, D.; Ren, S.; Feng, X. Transcriptome analysis of chlorantraniliprole resistance development in the diamondback moth Plutella xylostella. PLoS One, 2013, 8, e72314.
[114]
Li, X.; Zhu, B.; Guo, L.; Liang, P. Over-expression of UDP-glycosyltransferase gene UGT2B17 is involved in chlorantraniliprole resistance in Plutella xylostella (L.). Pest Manag. Sci., 2017, 73, 1402-1409.
[115]
Ribeiro, L.M.S.; Wanderley-Teixeira, V.; Ferreira, H.N.; Teixeira, A.A.C.; Siqueira, H.A.A. Fitness costs associated with field-evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bull. Entomol. Res., 2014, 104, 88-96.


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VOLUME: 19
ISSUE: 1
Year: 2019
Page: [22 - 33]
Pages: 12
DOI: 10.2174/1389557518666180330112908
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