Golden age of RyR and GABA -R Diamide and Isoxazoline insecticides: Common genesis, serendipity, surprises, selectivity, and safety

Chemical Research in Toxicology

Volumn 28, Issue 4, 2015, Pages 560-566

  Casida, John E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; DIAMIDE; INSECTICIDE; ISOXAZOLINE DERIVATIVE; RYANODINE RECEPTOR; ISOXAZOLE DERIVATIVE;

ARTICLE; CALCIUM TRANSPORT; CHEMICAL SAFETY; CROP PROTECTION; CROSS RESISTANCE; INSECT CONTROL; INSECTICIDAL ACTIVITY; NONHUMAN; PEST MANAGEMENT; PROTEIN TARGETING; ANIMAL; CAT; DOG; DRUG EFFECTS;

CANIS FAMILIARIS; HEXAPODA; IXODIDA; MAMMALIA; SIPHONAPTERA (FLEAS);

ANIMALS; CATS; DIAMIDE; DOGS; INSECTICIDES; ISOXAZOLES; RECEPTORS, GABA; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84928116531     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx500520w     Document Type: Article

References (81)

1. Casida, J. E. and Quistad, G. B. (1998) Golden age of insecticide research: past, present or future? Annu. Rev. Entomol. 43, 1-16
2. Casida, J. E. and Durkin, K. A. (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects Annu. Rev. Entomol. 58, 99-117
3. Tohnishi, M., Nakao, H., Kohno, E., Nishidi, T., Furuya, T., Shimizu, T., Seo, A., Sakata, K., Fujioka, S., and Kanno, H. (2003) Phthalamide Derivatives, or Salt Thereof Agrohorticultural Insecticide, and Method for Using the Same, U.S. Patent 6603044 B1.
4. Tohnishi, M., Nakao, H., Furuya, T., Seo, A., Kodama, H., Tsubata, K., Fujioka, S., Kodama, H., Hirooka, T., and Nishimatsu, T. (2005) Flubendiamide, a novel insecticide highly active against lepidopterous insect pests J. Pestic. Sci. 30, 354-360
5. Nauen, R. (2006) Insecticide mode of action: return of the ryanodine receptor Pest Manag. Sci. 62, 690-692
6. Jeanguenat, A. (2012) The story of a new insecticidal chemistry class: the diamides Pest Manag. Sci. 69, 7-14
7. Lahm, G. P., Selby, T. P., Freudenberger, J. H., Stevenson, T. M., Myers, B. J., Seburyamo, G., Smith, B. K., Flexner, L., Clark, C. E., and Cordova, D. (2005) Insecticidal anthranilic diamides: a new class of potent ryanodine receptor activators Bioorg. Med. Chem. Lett. 15, 4898-4906
8. Lahm, G. P., Stevenson, T. M., Selby, T. P., Freudenberger, J. H., Dubas, C. M., Smith, B. K., Cordova, D., Flexner, L., Clark, C. E., Bellin, C. A., and Hollingshaus, J. G. (2007) Rynaxypyr: A New Anthranilic Diamide Insecticide Acting at the Ryanodine Receptor, in Pesticide Chemistry: Crop Protection, Public Health, Environmental Safety (Ohkawa, H., Miyagawa, H., and Lee, P. W., Eds.) pp 111-120, Wiley, Weinheim, Germany.
9. Lahm, G. P., Cordova, D., and Barry, J. D. (2009) New and selective ryanodine receptor activators for insect control Bioorg. Med. Chem. 17, 4127-4133
10. Lahm, G. P., Myers, B. J., Selby, T. P., and Stevenson, T. M. (2001) Arthropodicides, U.S. Patent 6747047 B2.
11. Hughes, K. A., Lahm, G. P., Selby, T. P., and Stevenson, T. M. (2004) Cyano Anthranilamide Insecticides, U.S. Patent 7247647 B2.
12. Pepper, B. P. and Carruth, L. A. (1945) A new plant insecticide for control of the European corn borer J. Econ. Entomol. 38, 59-66
13. Casida, J. E., Pessah, I. N., Seifert, J., and Waterhouse, A. L. (1987) Ryania Insecticide: Chemistry, Biochemistry and Toxicology, in Pesticide Science and Biotechnology (Greenhalgh, R. and Roberts, T. R., Eds.) pp 177-182, Blackwell, Oxford, England.
14. Wiesner, K. (1972) The structure of ryanodine Adv. Org. Chem. 8, 295-316
15. Waterhouse, A. L., Holden, I., and Casida, J. E. (1984) 9,21-Didehydroryanodine: a new principal toxic constituent of the botanical insecticide Ryania J. Chem. Soc., Chem. Commun. 19, 1265-1266
16. Pessah, I. N., Waterhouse, A. L., and Casida, J. E. (1985) The calcium ryanodine receptor complex of skeletal and cardiac muscle Biochem. Biophys. Res. Commun. 128, 449-456
17. 2+, caffeine and adenine nucleotides Mol. Pharmacol. 31, 232-238
18. Sutko, J. L., Airey, J. A., Welch, W., and Ruest, L. (1997) The pharmacology of ryanodine and related compounds Pharmacol. Rev. 49, 53-98
19. Welch, W. (2002) Quantitative relationships between ryanoids, receptor affinity and channel conductance Front. Biosci. 7, 1727-1742
20. Wehrens, X. H. T. and Marks, A. R., Eds. (2005) Ryanodine Receptors: Structure, Function and Dysfunction in Clinical Diseases, pp 330, Springer, New York.
21. Sattelle, D. B., Cordova, D., and Cheek, T. R. (2008) Insect ryanodine receptors: molecular targets for novel pest control chemicals Invertebr. Neurosci. 3, 107-119
22. Lehmberg, E. and Casida, J. E. (1994) Similarity of insect and mammalian ryanodine binding sites Pestic. Biochem. Physiol. 48, 145-152
23. Jefferies, P. R. and Casida, J. E. (1994) Ryanoid chemistry and action Am. Chem. Soc. Symp. Ser. 551, 130-144
24. Jefferies, P. R., Yu, P., and Casida, J. E. (1997) Structural modifications increase the insecticidal activity of ryanodine Pestic. Sci. 51, 33-38
25. Waterhouse, A. L., Pessah, I. N., Francini, A. O., and Casida, J. E. (1987) Structural aspects of ryanodine action and selectivity J. Med. Chem. 30, 710-716
26. Casida, J. E. (1987) Serendipity in Pesticide Mode of Action and Metabolism, in A New Turn in Pesticide Sciences (Eto, M., Ed.) pp 115-144, Soft Science Publications, Tokyo, Japan.
27. Masaki, T. (2006) New insecticide affecting ryanodine receptor, flubendiamide: biochemical aspects of its action Nippon Noyaku Gakkaishi 31, 484-488
28. 2+ release Mol. Pharmacol. 69, 1733-1739
29. 2+ release channels in insects Cell Calcium 39, 21-33
30. Lümmen, P., Ebbinghaus-Kintscher, U., Funke, C., Fischer, R., Masaki, T., Yasokawa, N., and Tohnishi, M. (2007) Phthalic acid diamides activate insect ryanodine receptors Am. Chem. Soc. Symp. Ser. 948, 235-248
31. 2+ Pump Activity Coupled to RyR-Mediated Calcium Release in Lepidopterous Insects, in Pesticide Chemistry: Crop Protection, Public Health, Environmental Safety (Ohkawa, H., Miyagawa, H., and Lee, P. W., Eds.) pp 137-140, Wiley, Weinheim, Germany.
32. Ebbinghaus-Kintscher, U., Lümmen, P., Raming, K., Masaki, T., and Yasokawa, N. (2007) Flubendiamide, the first insecticide with a novel mode of action on insect ryanodine receptors Pflanzenschutz-Nachr. Bayer (Engl. Ed.) 60, 117-140
33. 2+ release channel Biochemistry 48, 10342-10352
34. 2+ pump stimulation by flubendiamide and its related compounds J. Pestic. Sci. 34, 37-42
35. Hamaguchi, H., Hirooka, T., and Masaki, T. (2012) Ryanodine Receptor Modulators: Diamides, in Modern Crop Protection Compounds (Kramer, W., Schirmer, U., Jeschke, P., and Witschel, M., Eds.) 2 nd ed., pp 1389-1396, Wiley, Weinheim, Germany.
36. Hamaguchi, H. and Hirooka, T. (2012) Flubendiamide, in Modern Crop Protection Compounds (Kramer, W., Schirmer, U., Jeschke, P., and Witschel, M., Eds.) 2 nd ed., pp 1396-1409, Wiley, Weinheim, Germany.
37. 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., and Tao, Y. (2006) Anthranilic diamides: a new class of insecticides with a novel mode of action, ryanodine receptor activation Pestic. Biochem. Physiol. 84, 196-214
38. Lahm, G., Stevenson, T., Selby, T., Freudenberger, J., Cordova, D., Flexner, L., Bellin, C., Smith, B., Hughes, K., Hollingshaus, J., Clark, C., and Benner, E. (2007) Rynaxypyr: a new insecticidal anthranilic diamide that acts as a potent and selective ryanodine receptor activator Bioorg. Med. Chem. Lett. 17, 6274-6279
39. 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., Caspar, T., Ragghianti, J. J., Gutteridge, S., Rhoades, D. F., Wu, L., Smith, R. M., and Tao, Y. (2007) Elucidation of the Mode of Action of Rynaxypyr, a Selective Ryanodine Receptor Activator, in Pesticide Chemistry: Crop Protection, Public Health, Environmental Safety (Ohkawa, H., Miyagawa, H., and Lee, P. W., Eds.) pp 121-126, Wiley, Weinheim, Germany.
40. 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., and Tao, Y. (2007) The novel mode of action of anthranilic diamide insecticides: ryanodine receptor activation Am. Chem. Soc. Symp. Ser. 948, 223-234
41. 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., and Pahutski, T. F. (2013) Discovery of cyantraniliprole, a potent and selective anthranilic diamide ryanodine receptor activator with cross-spectrum insecticidal activity Bioorg. Med. Chem. Lett. 23, 6341-6345
42. Lümmen, P. (2013) Calcium channels as molecular targets of novel insecticides Adv. Insect Physiol. 44, 287-347
43. 3H]ryanodine Chem. Res. Toxicol. 25, 1571-1573
44. Qi, S. and Casida, J. E. (2013) Species differences in chlorantraniliprole and flubendiamide insecticide binding sites in the ryanodine receptor Pestic. Biochem. Physiol. 107, 321-326
45. Qi, S., Lümmen, P., Nauen, R., and Casida, J. E. (2014) Diamide insecticide target site specificity in the Heliothis and Musca ryanodine receptors relative to toxicity J. Agric. Food Chem. 62, 4077-4082
46. Caspar, T., Cordova, D., Gutteridge, S., Rauh, J. J., Smith, R. M., Wu, L., and Tao, Y. (2003) Isolation and Use of Ryanodine Receptors, WO Patent 2004027042.
47. Gutteridge, S., Caspar, T., Cordova, D., Rauh, J. J., Smith, R. J., Wu, L., and Tao, Y. (2003) Ryanodine Receptor Polypeptides, U.S. Patent 8101715 B2.
48. Kato, K., Kiyonaka, S., Masaki, T., Mizuno, Y., Mori, E., and Mori, Y. (2007) Silkworm Ryanodine Receptor Protein, cDNA Thereof, Recombinant Vector, Expression Plasmid, Cell Showing Constant Expression, Method of Screening Insecticidal Component and Method of Screening Substance Reacting with Silkworm Ryanodine Receptor. WO Patent 2007094408 A1.
49. Wang, X., Wu, S., Yang, Y., and Wu, Y. (2012) Molecular cloning, characterization and mRNA expression of a ryanodine receptor gene from diamondback moth Plutella xylostella Pestic. Biochem. Physiol. 102, 204-212
50. Troczka, B., Zimmer, C. T., Elias, J., Schorn, C., Bass, C., Davies, T. G., Field, L. M., Williamson, M. S., Slater, R., and Nauen, R. (2012) 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. Bol. 42, 873-880
51. Lin, Q., Jin, F., Hu, Z., Chen, H., Yin, F., Li, Z., Dong, X., Zhang, D., Ren, S., and Feng, X. (2013) Transcriptome analysis of chlorantraniliprole resistance development in the diamondback moth Plutella xylostella PLoS One 8 (8) e72314 10.1371/journal.pone.0072314
52. Gong, W., Yan, H. H., Gao, L., Guo, Y. Y., and Xue, C. B. (2014) Chlorantraniliprole resistance in the diamondback moth (Lepidoptera: Plutellidae) J. Econ. Entomol. 107, 806-814
53. Tao, Y., Gutteridge, S., Benner, E. A., Wu, L., Rhoades, D. F., Sacher, M. D., Rivera, M. A., Desaeger, J., and Cordova, D. (2013) Identification of a critical region in the Drosophila ryanodine receptor that confers sensitivity to diamide insecticides Insect Biochem. Mol. Biol. 43, 820-828
54. Lahm, G. P., Cordova, D., Barry, J. D., Pahutski, T. F., Smith, B. K., Long, J. K., Benner, E. A., Holyoke, C. W., Joraski, K., Xu, M., Schroeder, M. E., Wagerle, T., Mahaffey, M. J., Smith, R. M., and Tong, M. H. (2013) 4-Azolylphenyl isoxazoline insecticides acting at the GABA gated chloride channel Bioorg. Med. Chem. Lett. 23, 3001-3006
55. Shoop, W. L., Hartline, E. J., Gould, B. R., Waddell, M. E., McDowell, R. G., Kinney, J. B., Lahm, G. P., Long, J. K., Xu, M., Wagerle, T., Jones, G. S., Dietrich, R. F., Cordova, D., Schroeder, M. E., Rhoades, D. F., Benner, E. A., and Confalone, P. N. (2014) Discovery and mode of action of afoxolaner, a new isoxazoline parasiticide for dogs Vet. Parasitol. 201, 179-189
56. Mita, T., Kudo, Y., Mizukoshi, T., Hotta, H., Maeda, H., and Takii, S. (2004) Substituted Benzanilide Compound and Pest Control Agent, WO Patent 2004018410.
57. Mita, T., Kikuchi, T., Mizukoshi, T., Yaosaka, M., and Komoda, M. (2005) Isoxazoline-Substituted Benzamide Compound and Noxious Organism Control Agent, WO Patent 2005085216 A1.
58. Ozoe, Y., Asahi, M., Ozoe, F., Nakahira, K., and Mita, T. (2010) The antiparasitic isoxazoline A1443 is a potent blocker of insect ligand- gated chloride channels Biochem. Biophys. Res. Commun. 391, 744-749
59. Lahm, G. P., Shoop, W. L., and Xu, M. (2011) Isoxazolines for Controlling Invertebrate Pests, EP Patent 1973888 B1.
60. Freehauf, K., Waldron, N., Lutz, J., and Guerino, F. (2013) Solid Oral Pharmaceutical Compositions for Isoxazoline Compounds, WO Patent 150055 A1.
61. Yoshida, K., Wakita, T., Katsuta, H., Kai, A., Chiba, Y., Takahashi, K., Kato, H., Kawahara, N., Nomura, M., Daido, H., Maki, J., and Banba, S. (2014) Amide Derivatives, Process for Preparation Thereof and Use Thereof As Insecticide, U.S. Patent 0206727A1.
62. Nakao, T., Banba, S., Nomura, M., and Hirase, K. (2013) Meta-diamide insecticides acting on distinct sites of RDL GABA receptor from those for conventional noncompetitive antagonists Insect Biochem. Mol. Biol. 43, 366-375
63. Nakao, T. and Hirase, K. (2013) A comparison of the modes of action of novel meta-diamide insecticides and conventional noncompetitive antagonists on the Spodoptera litura RDL GABA receptor J. Pestic. Sci. 38, 123-128
64. Ozoe, Y., Kita, T., Ozoe, F., Nakao, T., Sato, K., and Hirase, K. (2013) Insecticidal 3-benzamido- N -phenylbenzamides specifically bind with high affinity to a novel allosteric site in housefly GABA receptors Pestic. Biochem. Physiol. 107, 285-292
65. Nakao, T. and Banba, S. (2014) Minireview: mode of action of meta-diamide insecticides. Pestic. Biochem. Physiol. DOI: 10.1016/j.pestbp.2014.09.010.
66. Casida, J. E. (1993) Insecticide action at the GABA-gated chloride channel: recognition, progress, and prospects Arch. Insect Biochem. Physiol. 22, 13-23
67. Buckingham, S. D., Biggin, P. C., Sattelle, B. M., Brown, L. A., and Sattelle, D. B. (2005) Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides Mol. Pharmacol. 68, 942-951
68. Ozoe, Y., Takeda, M., and Matsuda, K. (2009) γ-Aminobutyric Acid Receptors: A Rationale for Developing Selective Insect Pest Control Chemicals, in Biorational Control of Arthropod Pests (Ishaaya, S. and Horowitz, A. R., Eds.) pp 131-162, Springer, New York.
69. Ozoe, Y. (2013) γ-Aminobutyrate- and glutamate-gated chloride channels as targets of insecticides Adv. Insect Physiol. 44, 211-286
70. Casida, J. E. and Durkin, K. A. (2014) Novel GABA Receptor Pesticide Targets, Pestic. Biochem. Physiol. DOI: 10.1016/j.pestbp.2014.11.006.
71. Chen, L., Durkin, K. A., and Casida, J. E. (2006) Structural model for γ- aminobutyric acid receptor noncompetitive antagonist binding: Widely diverse structures fit the same site Proc. Natl. Acad. Sci. U.S.A. 103, 5185-5190
72. ffrench-Constant, R. H., Daborn, P. J., and Le Goff, G. (2004) The genetics and genomics of insecticide resistance Trends Genet. 20, 163-170
73. 3H]EBOB binding site associated with Ala→Ser or Gly mutants of Rdl subunit Life Sci. 56, 757-765
74. 3H]isoxazoline insecticide Chem. Res. Toxicol. 26, 514-516
75. 3H]avermectin J. Agric. Food Chem. 62, 1019-1024
76. Gassel, M., Wolf, C., Noack, S., Williams, H., and Ilg, T. (2014) The novel isoxazoline ectoparasiticide fluralaner: selective inhibition of arthropod γ-aminobutyric acid- and L-glutamate-gated chloride channels and insecticidal/acaricidal activity Insect Biochem. Mol. Biol. 45, 111-124
77. Kilp, S., Ramirez, D., Allan, M. J., Roepke, R. K. A., and Nuernberger, M. C. (2014) Pharmacokinetics of fluralaner in dogs following a single oral or intravenous administration Parasites Vectors 7, 85
78. Long, J. K., Selby, T. P., and Xu, M. (2013) Napthalene Isoxazoline Compounds for Control of Invertebrate Pests, U.S. Patent 8367584.
79. Beugnet, F., deVos, C., Liebenberg, J., Halos, L., and Fourie, J. (2014) Afoxolaner against fleas: immediate efficacy and resultant mortality after short exposure on dogs Parasite 21, 42
80. Letendre, L., Huang, R., Kvaternick, V., Harriman, J., Drag, M., and Soll, M. (2014) The intraveneous and oral pharmacokinetics of afoxolaner used as a monthly chewable antiparasitic for dogs Vet. Parasitol. 201, 190-197
81. Nauen, R., Elbert, A., Mccaffery, A., Slater, R., and Sparks, T. C. (2012) IRAC: Insecticide Resistance and Mode of Action Classification of Insecticides, in Modern Crop Protection Compounds (Kramer, W., Schirmer, U., Jeschke, P., and Witschel, M., Eds.) 2 nd ed., pp 935-956, Wiley, Weinheim, Germany.