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GABA and Glutamate Receptors as Biochemical Sites for Insecticide Action

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Biochemical Sites of Insecticide Action and Resistance

Abstract

The γ-aminobutyric acid (GABA) receptor/chloride ionophore complex has been the focus of intense interest by industrial and academic scientists as a site of insecticide action (Bloomquist 1993). This receptor was initially exploited as a site of action for commercial insecticides over 40 years ago by the polychlorocycloalkane compounds (e.g., cyclodienes, toxaphene, and lindane), although the suggestion that they might be disrupting GABA receptor function was not advanced until 1982 (Ghiasuddin and Matsumura 1982). This hypothesis was roughly contemporaneous with the discovery of the avermectins, which were originally hypothesized to affect GABA-gated chloride channels, but now are thought to mainly affect the glutamate-gated chloride channel of invertebrate muscle (Rohrer and Arena 1995).

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References

  • Albert J, Lingle C, Marder E, O’Neil M (1986) A GABA–activated chloride–conductance not blocked by picrotoxin on spiny lobster neuromuscular preparations. Br J Pharmacol 87:771–779.

    PubMed  CAS  Google Scholar 

  • Andreev D, Kreitman M, Phillips T, Beeman R, ffrench-Constant R (1999) Multiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae). J Mol Evol 48:615–624.

    Article  PubMed  CAS  Google Scholar 

  • Anthony N, Holyoke C Jr, Sattelle D (1994) Blocking actions of picrotoxinin analogues on insect (Periplaneta americana) GABA receptors. Neurosci Lett 171:67–69.

    Article  PubMed  CAS  Google Scholar 

  • Bai D, Sattelle D (1995) A GABAB receptor on an identified insect motor neurone. J Exp Biol 198:889–894.

    PubMed  CAS  Google Scholar 

  • Blackhall W, Pouliot J-F, Prichard R, Beech R (1998) Haemonchus contortus: selection at a glutamate–gated chloride channel gene in ivermectin– and moxidectin–selected strains. Exp Parasitol 90:42–48.

    Article  PubMed  CAS  Google Scholar 

  • Bloomquist J (1993) Toxicology, mode of action, and target site–mediated resistance to insecticides acting on chloride channels. Comp Biochem Physiol 106C:301–314.

    CAS  Google Scholar 

  • Bloomquist J (1994) Cyclodiene resistance at the insect GABA receptor/chloride channel complex confers broad cross resistance to convulsants and experimental phenylpyrazole insecticides. Arch Insect Biochem Physiol 26:69–79.

    Article  PubMed  CAS  Google Scholar 

  • Bloomquist J (1998) Chemistry and toxicology of the chlorinated cyclodienes and lindane. Rev Toxicol 2:333–355.

    CAS  Google Scholar 

  • Bloomquist J, Robinson W (1999) Prevalence and magnitude of resistance to cyclodiene and phenylpyrazole insecticides in Blattella germanica and Drosophila melanogaster. In: Robinson W, Rettich F, Rambo G (eds) Proceedings of the 3rd international conference on insect pests in the urban environment. Graficke zavody Hronov, Czech Republic, pp 27–34.

    Google Scholar 

  • Bloomquist J, Grubs R, Soderlund D, Knipple D (1991) Prolonged exposure to GABA activates GABA–gated chloride channels in the presence of channel–blocking convulsants. Comp Biochem Physiol 99C:397–402.

    CAS  Google Scholar 

  • Bloomquist J, Jackson J, Karr L, Ferguson H, Gajewski R (1993) Spirosultam LY219048: a new chemical class of neurotoxin acting upon the GABA receptor/chloride ionophore complex. Pestic Sci 39:185–192.

    Article  CAS  Google Scholar 

  • Buckingham S, Hosie A, Roush R, Sattelle D (1994) Actions of agonists and convulsant antagonists on a Drosophila melanogaster GABA receptor (Rdl) homo–oligomer expressed in Xenopus oocytes. Neurosci Lett 181:137–140.

    Article  PubMed  CAS  Google Scholar 

  • Casida J (1993) Insecticide action at the GABA–gated chloride channel: recognition, progress, and prospects. Arch Insect Biochem Physiol 22:13–23.

    Article  PubMed  CAS  Google Scholar 

  • Casida J, Nicholson R, Palmer C (1988) Trioxabicyclooctanes as probes for the convulsant site of the GABA–gated chloride channel in mammals and arthropods. In: Lunt GG (ed) Neurotox’88: molecular basis of drug and pesticide action. Elsevier, Amsterdam, pp 125–144.

    Google Scholar 

  • Clark J, Scott J, Campos F, Bloomquist J (1995) Resistance to avermectins: extent, mechanisms, and management implications. Annu Rev Entomol 40:1–30.

    Article  PubMed  CAS  Google Scholar 

  • Cleland T (1996) Inhibitory glutamate receptor channels. Mol Neurobiol 13:97–136.

    Article  PubMed  CAS  Google Scholar 

  • Cole L, Nicholson R, Casida J (1993) Action of phenylpyrazole insecticides at the GABA–gated chloride channel. Pestic Biochem Physiol 46:47–54.

    Article  CAS  Google Scholar 

  • Cole L, Saleh M, Casida J (1994) Housefly head GABA–gated chloride channel: [3H]α–endosulfan binding in relation to polychlorocycloalkane insecticide action. Pestic Sci 42:59–63.

    Article  CAS  Google Scholar 

  • Corronc H, Hue B (1999) A native picrotoxin–resistant GABA–gated chloride channel receptor subtype in cockroach neurons. Pestic Sci 55:1007–1011.

    Article  Google Scholar 

  • Cully D, Vassilatis K, Liu K, Paress P, Van der Ploeg L, Schaeffer J, Arena J (1994) Cloning of an avermectin–sensitive glutamate–gated chloride channel from Caenorhabditis elegans. Nature 371:707–711.

    Article  PubMed  CAS  Google Scholar 

  • Cully D, Paress P, Liu K, Schaeffer J, Arena J (1996) Identification of a Drosophila melanogaster Drosophila melanogaster glutamate–gated chloride channel sensitive to the antiparasitic agent avermectin. J Biol Chem 271:20187–20191.

    Article  PubMed  CAS  Google Scholar 

  • Darlison M (1992) Invertebrate GABA and glutamate receptors: molecular biology reveals predictable structures but some unusual pharmacologies. Trends Neurosci 15:469–474.

    Article  PubMed  CAS  Google Scholar 

  • Deng Y (1995) Insecticide binding sites in the housefly head γ–aminobutyric acid gated chloride– channel complex. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp 230–250.

    Google Scholar 

  • Duce I, Bhandal N, Scott R, Norris T (1995) Effects of ivermectin on γ–aminobutyric acid and glutamate–gated chloride conductance in arthropod skeletal muscle. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp 250–263.

    Google Scholar 

  • Eichenseer H, Mullin C, Chyb S (1998) Antifeedant discrimination thresholds for two populations of western corn rootworm. Physiol Entomol 23:220–226.

    Article  CAS  Google Scholar 

  • Etter A, Cully D, Liu K, Reiss B, Vassilatis D, Schaeffer J, Arena J (1999) Picrotoxin blockade of invertebrate glutamate–gated chloride channels: subunit dependence and evidence for binding within the pore. J Neurochem 72:318–326.

    PubMed  CAS  Google Scholar 

  • ffrench-Constant R, Roush R (1991) Gene mapping and cross–resistance in cyclodiene insecticide–resistant Drosophila melanogaster (Mg.). Genet Res Camb 57:17–21.

    Article  CAS  Google Scholar 

  • ffrench-Constant R, Zhang H-J, Jackson M (1995) Biophysical analysis of a single amino acid replacement in the resistance to dieldrin γ–aminobutyric acid receptor. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp 192–204.

    Google Scholar 

  • ffrench-Constant R, Anthony N, Andreev D, Aronstein K (1996) Single versus multiple origins of insecticide resistance: inferences from the cyclodiene resistance gene Rdl. In: Brown T (ed) Molecular genetics and evolution of pesticide resistance. ACS Symp Ser 645:106–116.

    Article  CAS  Google Scholar 

  • Fischer M, Mrozik H (1992) The chemistry and pharmacology of avermectins. Annu Rev Pharmacol Toxicol 32:537–553.

    Article  Google Scholar 

  • Gant D, Chalmers A, Wolff M, Hoffman H, Bushey D (1998) Fipronil: action at the GABA receptor. Rev Toxicol 2:147–156.

    CAS  Google Scholar 

  • Ghiasuddin S, Matsumura F (1982) Inhibition of gamma–aminobutyric acid (GABA)–induced chloride uptake by gamma–BHC and heptachlor epoxide. Comp Biochem Physiol 73C:141–144.

    CAS  Google Scholar 

  • Gonzalez-Coloma A, Gutierrez C, Cabrera R, Reina M (1997) Silphinene derivatives: their effects and modes of action on Colorado potato beetle. J Agric Food Chem 45:946–950.

    Article  CAS  Google Scholar 

  • Goudie A, Evans N, Gration K, Bishop B, Gibson S, Holdom K, Kaye B, Wicks S, Lewis D, Weatherly A, Bruce C, Herbert A, Seymour D (1993) Doramectin – a potent novel endectocide. Vet Parasitol 49:5–15.

    Article  PubMed  CAS  Google Scholar 

  • Hainzl D, Casida J (1996) Fipronil insecticide: novel photochemical desulfinylation with retention of neurotoxicity. Proc Natl Acad Sci USA 93:12764–12767.

    Article  PubMed  CAS  Google Scholar 

  • Hainzl D, Cole L, Casida J (1998) Mechanisms for selective toxicity of fipronil insecticide and its sulfone metabolite and desulfinyl photoproduct. Chem Res Toxicol 11:1529–1535.

    Article  PubMed  CAS  Google Scholar 

  • Holden-Dye L, Walker R (1990) Avermectin and avermectin derivatives are antagonists at the 4–aminobutyric acid (GABA) receptor on the somatic muscle cells of Ascaris; is this the site of anthelmintic action? Parasitology 101:265–271.

    Article  PubMed  CAS  Google Scholar 

  • Hosie A, Baylis H, Duckingham S, Sattelle D (1995a) Actions of the insecticide fipronil on dield– rin–sensitive and –resistant GABA receptors of Drosophila melanogaster. Br J Pharmacol 115:909–912.

    PubMed  CAS  Google Scholar 

  • Hosie A, Shirai Y, Buckingham S, Rauh J, Roush R, Baylis H, Sattelle D (1995b) Blocking actions of BIDN, a bicyclic dinitrile convulsant compound, on wild–type and dieldrin–resistant GABA receptor homo–oligomers of Drosophila melanogaster expressed in Xenopus oocytes. Brain Res 693:257–260.

    Article  PubMed  CAS  Google Scholar 

  • Hosie A, Ozoe Y, Koike K, Ohmoto T, Nikaido T, Sattelle D (1996) Actions of picrodendrin antagonists on dieldrin–sensitive and –resistant Drosophila GABA receptors. Br J Pharmacol 119:1569–1576.

    PubMed  CAS  Google Scholar 

  • Hosie A, Aronstein K, Sattelle D, ffrench-Constant R (1997) Molecular biology of insect neuronal GABA receptors. Trends Neurosci 20:578–583.

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Casida J (1996) Characterization of [3H]ethynylbicycloorthobenzoate ([3H]EBOB) binding and the action of insecticides on the γ–aminobutyric acid–gated chloride channel in cultured cerebellar granule neurons. J Pharmacol Exp Ther 279:1191–1196.

    PubMed  CAS  Google Scholar 

  • Huang J, Casida J (1997a) Role of cerebellar granule cell–specific GABAA receptor subtype in the differential sensitivity of [3H]ethynylbicycloorthobenzoate binding to GABA mimetics. Neurosci Lett 225:85–88.

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Casida J (1997b) Avermectin Bla binds to high– and low–affinity sites with dual effects on the γ–aminobutyric acid–gated chloride channel of cultured cerebellar granule neurons. J Pharmacol Exp Ther 281:261–266.

    PubMed  CAS  Google Scholar 

  • Hue B (1991) Functional assay for GABA receptor subtypes of a cockroach giant interneuron.Arch Insect Biochem Physiol 18:147–157.

    Google Scholar 

  • Ikeda T, Nagata K, Shono T, Narahashi T (1998) Dieldrin and picrotoxinin modulation of GABAA receptor single channels. NeuroReport 9:3189–3195.

    PubMed  CAS  Google Scholar 

  • Ju X, Ozoe Y (1999) Bicyclophosphorothionate antagonists exhibiting selectivity for housefly GABA receptors. Pestic Sci 55:971–982.

    Article  CAS  Google Scholar 

  • Kaku K, Matsumura F (1995) Chloride–channel gene probes from cyclodiene–resistant and – susceptible strains of Blattella germanica. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp 216–229.

    Google Scholar 

  • Knipple D, Henderson J, Soderlund D (1995) Structural and functional characterization of insect genes encoding ligand-gated chloride–channel subunits. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp 205–215.

    Google Scholar 

  • Lummis S (1990) GABA receptors in insects. Comp Biochem Physiol 95C:l–8.

    Google Scholar 

  • Matsuda K, Hosie A, Holyoke C Jr, Rauh J, Sattelle D (1999) Cross–resistance with dieldrin of a novel tricyclic dinitrile GABA receptor antagonist. Br J Pharmacol 127:1305–1307.

    Article  PubMed  CAS  Google Scholar 

  • Meinke P, Shoop W, Michael B, Blizzard T, Dawson G, Fisher M, Mrozik H (1998) Synthesis of gem– difluoroavermectin derivatives: potent anthelmintic and anticonvulsant agents. Bioorg Med Chem Lett 8:3643–3646.

    Article  PubMed  CAS  Google Scholar 

  • Mullin C, Chyb S, Eichenseer H, Hollister B, Frazier J (1994) Neuroreceptor mechanisms in insect gustation: a pharmacological approach. J Insect Physiol 40:913–931.

    Article  CAS  Google Scholar 

  • Mullin C, Gonzalez-Coloma A, Gutierrez C, Reina M, Eichenseer H, Hollister B, Chyb S (1997) Antifeedant effects of some novel terpenoids on Chrysomelidae beetles: comparisons with alkaloids on an alkaloid–adapted and nonadapted species. J Chem Ecol 23:1851–1866.

    Article  CAS  Google Scholar 

  • Narahashi T, Ginsburg K, Nagata K, Song J, Tatebayashi H (1998) Ion channels as targets for insecticides. NeuroToxicol 19:581–590.

    CAS  Google Scholar 

  • Newland C, Cull-Candy S (1992) On the mechanism of action of picrotoxin on GABA receptor channels in dissociated sympathetic neurones of the rat. J Physiol (Lond) 447:191–231.

    CAS  Google Scholar 

  • Oppenoorth FJ (1985) Biochemistry and genetics of insecticide resistance. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect biochemistry, physiology, and pharmacology, vol 12. Pergamon Press, Oxford, pp 731–773.

    Google Scholar 

  • Ozoe Y, Matsumoto K, Mochida K, Nakamura T (1995) Six-membered cyclic phosphonate GABA antagonists: 2,5–disubstituted 1,3,2–dioxaphosphorinanes. Biosci Biotech Biochem 59: 2314–2316.

    Article  CAS  Google Scholar 

  • Ozoe Y, Arkamatsu M, Higata T, Ikeda I, Mochida K, Koike K, Ohmoto T, Nikaido T (1998a) Picro– dendrin and related terpenoid antagonists reveal structural differences between ionotropic GABA receptors of mammals and insects. Bioorg Med Chem 6:481–492.

    Article  PubMed  CAS  Google Scholar 

  • Ozoe Y, Niina K, Matsumoto K, Ikeda I, Mochida K, Ogawa C, Matsuno A, Miki M, Yanagi K (1998b) Actions of cyclic esters, S–esters, and amides of phenyl– and phenylthiophosphonic acids on mammalian and insect GABA–gated chloride channels. Bioorg Med Chem 6:73–83.

    Article  PubMed  CAS  Google Scholar 

  • Palmer C, Casida J (1995) Insecticidal 1,3–oxathianes and their oxides. J Agric Food Chem 43:498–502.

    Article  CAS  Google Scholar 

  • Pulman D, Smith I, Larkin J, Casida J (1996) Heterocyclic insecticides acting at the GABA–gated chloride channel: 5–alkyl–2–arylpyrimidines and –1,3–thiazines. Pestic Sci 46:237–245.

    Article  CAS  Google Scholar 

  • Putter I, Mac Connell J, Preiser F, Haidiri A, Ristich S, Dybas R (1981) Avermectins: novel insecticides, acaricides, and nematicides from a soil microorganism. Experientia 37:963–964.

    Article  CAS  Google Scholar 

  • Rauh J, Lummis S, Sattelle D (1990) Pharmacological and biochemical properties of insect GABAreceptors. Trends Pharmacol Sci 11:325–329.

    Article  PubMed  CAS  Google Scholar 

  • Rauh J, Benner E, Schnee M, Cordova D, Holyoke C, Howard M, Bai D, Buckingham S, Hutton M, Hamon A, Roush R, Sattelle D (1997) Effects of [3H]BIDN, a novel bicyclic dinitrile radioligand for GABA–gated chloride channels of insects and vertebrates. Br J Pharmacol 121:1496–1505.

    Article  PubMed  CAS  Google Scholar 

  • Robertson B (1989) Actions of anaesthetics and avermectin on GABAA chloride channels in mammalian dorsal root ganglion neurones. Br J Pharmacol 98:167–176.

    PubMed  CAS  Google Scholar 

  • Rohrer S, Arena J (1995) Structural and functional characterization of insect genes encoding ligand–gated chloride–channel subunits. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp264–283.

    Google Scholar 

  • Sawicki R, Farnham A, Denholm I, Church V (1986) Potentiation of super-kdr resistance to deltamethrin and other pyrethroids by an intensifier (Factor 161) on autosome 2 in the housefly (Musca domestica L.). Pestic Sci 17:483–488.

    Article  CAS  Google Scholar 

  • Scott J (1995) Resistance to avermectins in the housefly, Musca domestica. In: Clark JM (ed) Molecular action of insecticides on ion channels. ACS Symp Ser 591. American Chemical Society, Washington, DC, pp 284–292.

    Google Scholar 

  • Scott J, Wen Z (1997) Toxicity of flpronil to susceptible and resistant strains of German cockroaches (Dictyoptera: Blattellidae) and houseflies (Diptera: Muscidae). J Econ Entomol 90:1152–1156.

    CAS  Google Scholar 

  • Shirai Y, Hosie A, Buckingham S, Holyoke C Jr, Baylis H, Sattelle D (1995) Actions of picrotoxinin analogues on an expressed, homo–oligomeric GABA receptor of Drosophila melanogaster. Neurosci Lett 189:1–4.

    Article  PubMed  CAS  Google Scholar 

  • Shoop W, Mrozik H, Fisher M (1995) Structure and activity of avermectins and milbemycins in animal health. Vet Parasitol 59:139–156.

    Article  PubMed  CAS  Google Scholar 

  • Valles S, Koehler P, Brenner R (1997) Antagonism of flpronil toxicity by piperonyl butoxide and S, S, S–tributyl phosphorotrithioate in the German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 90:1254–1258.

    CAS  Google Scholar 

  • Vassilatis D, Elliston K, Paress P, Hamelin M, Arena J, Schaeffer J, Van der Ploeg L, Cully D (1997) Evolutionary relationship of the ligand-gated ion channels and the avermectin-sensitive, glutamate-gated chloride channels. J Mol Evol 44:501–508

    Article  PubMed  CAS  Google Scholar 

  • Walker L, Bloomquist J (1999) Pharmacology of contractile responses in the alimentary system of caterpillars: implications for insecticide development and mode of action. Annu Ent Soc Am 92:902–908.

    CAS  Google Scholar 

  • Weston J, Larkin J, Pulman D, Holden I, Casida J (1995) Insecticidal isomers of 4-tert-butyl-1-(4-ethynylcyclohexyl)-2,6,7-trioxabicyclo [2.2.2] octane and 5-tert-butyl-2-(4- ethynylcyclohexyl)-l,3-dithiane. Pestic Sci 44:69–74.

    Article  CAS  Google Scholar 

  • Wolff M, Wingate V (1998) Characterization and comparative pharmacological studies of a functional γ–aminobutyric acid (GABA) receptor cloned from the tobacco budworm, Heliothis virescens (Noctuidae: Lepidoptera). Invertebr Neurosci 3:305–315.

    Article  CAS  Google Scholar 

  • Zhang H-G, ffrench-Constant R, Jackson M (1994) A unique amino acid of the Drosophila GABA receptor with influence on drug sensitivity by two mechanisms. J Physiol (Lond) 479:65–75.

    CAS  Google Scholar 

  • Zhang H-G, Lee H-J, Rocheleau T, ffrench-Constant R, Jackson M (1995) Subunit composition determines picrotoxin and bicuculline sensitivity of Drosophila γ-aminobutyric acid receptors. Mol Pharmacol 48:835–840.

    PubMed  CAS  Google Scholar 

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Bloomquist, J.R. (2001). GABA and Glutamate Receptors as Biochemical Sites for Insecticide Action. In: Ishaaya, I. (eds) Biochemical Sites of Insecticide Action and Resistance. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59549-3_2

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