Comparative Molecular Neurobiology pp 172-209

Part of the EXS book series (EXS, volume 63)

GABA Receptor molecules of insects

  • N. M. Anthony
  • J. B. Harrison
  • D. B. Sattelle

Summary

Receptors for 4-aminobutyric acid (GABA) have been identified in both central and peripheral nervous systems of several invertebrate phyla. To date, much of the information derived from physiological and biochemical studies on insect GABA receptors relates to GABA-gated chloride channels that show some similarities with vertebrate GABAA receptors. Like, their vertebrate central nervous system (CNS) counterparts, agonist activation of such insect GABA receptors leads to a rapid, picrotoxin-sensitive increase in chloride ion conductance across the cell membrane. In insects, responses to GABA can be modulated by certain benzodiazepines and barbiturates. However, recent studies have detected a number of striking pharmacological differences between GABA-gated chloride channels of insects and vertebrates. Receptor binding, electrophysiological and 36Cl flux assays have indicated that many insect receptors of this type are insensitive to the vertebrate GABAA antagonists bicuculline and pitrazepin. Benzodiazepine binding sites coupled to insect GABA receptors display a pharmacological profile distinct from that of corresponding sites in vertebrate CNS. Receptor binding studies have also demonstrated differences between convulsant binding sites of insect and vertebrate receptors.

Insect GABA receptor molecules are important target sites for several chemically-distinct classes of insecticidally-active molecules. By characterizing these pharmacological properties in detail, it may prove possible to exploit differences between vertebrate and insect GABA receptors in the rational design of novel, more selective pest control agents. The recent application of the powerful techniques of molecular biology has revealed a diversity of vertebrate GABAA receptor subunits and their respective isoforms that can assemble in vivo to form a multiplicity of receptor subtypes. Molecular cloning of insect GABA receptor subunits will not only enhance our understanding of invertebrate neurotransmitter receptor diversity but will also permit the precise identification of the sites of action of pest control agents.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abalis, I. M., Eldefrawi, M. E. and Eldefrawi, A. T. (1983) Biochemical identification of putative GABA/benzodiazepine receptors in housefly thorax muscles. Pestic. Biochem. Physiol. 20, 39–48.CrossRefGoogle Scholar
  2. Abalis, I. M., Eldefrawi, M. E. and Eldefrawi, A. T. (1985) Binding of GABA receptor channel drugs to a putative voltage-dependent chloride channel in Torpedo electric organ. Biochem. Pharmacol. 34, 2579–2582.CrossRefGoogle Scholar
  3. Abalis, I. M. and Eldefrawi, A. T. (1986) [3H]Muscimol binding to a putative GABA receptor in honey bee brain and its interaction with avermectin Bla. Pestic. Biochem. Physiol. 25, 279–287.Google Scholar
  4. Adams, P. R. and Brown, D. A. (1975) Actions of y-aminobutyric acid on rat sympathetic ganglion cells. J. Physiol. 250, 85–120.Google Scholar
  5. Akaike, N., Hattori, K., Oomura, Y. and Carpenter, D. O. (1985) Bicuculline and picrotoxin block γ-aminobutyric acid-gated Cl- conductance by different mechanisms. Experientia 41, 70–71.CrossRefGoogle Scholar
  6. Akaike, N., Inoue, M. and Krishtal, O. A. (1986) ‘Concentration clamp’ study of γ-aminobutyric-acid-induced chloride current kinetics in frog sensory neurones. J. Physiol. 379, 171–185.Google Scholar
  7. Allan, A. M. and Harris, R. A. (1986) γ-aminobutyric acid agonists and antagonists alter chloride flux across brain membranes. Mol. Pharmacol. 29, 497–505.Google Scholar
  8. Barker, J. L. and McBurney, R. N. (1979) Phenobarbitone modulation of postsynaptic GABA receptor function on cultured mammalian neurones. Proc. R. Soc. Lond. B206, 319–327.CrossRefGoogle Scholar
  9. Barker, J. L., Harrison, N. L., Lange, G. D. and Owen, D. G. (1987) Potentiation of γ-aminobutyric-acid-activated chloride conductance by a steroid anaesthetic in cultured rat spinal neurones. J. Physiol. 386, 485–501.Google Scholar
  10. Bermudez, I., Hawkins, C. A., Taylor, A. M. and Beadle, D. J. (1991) Actions of insecticides on the insect GABA receptor complex. J. Receptor Res. 11, 221–232.Google Scholar
  11. Betz, H. (1990) Ligand-gated ion channels in the brain: The amino acid receptor superfamily. Neuron 5, 383–392.CrossRefGoogle Scholar
  12. Blair, L. A. C., Levitan, E. S., Marshall, J., Dionne, V. E. and Barnard, E. A. (1988) Single subunits of the GABAA receptor form ion channels with properties of the native receptor. Science 242, 577–579.CrossRefGoogle Scholar
  13. Bloom, F. E. and Iversen, L. L. (1971) Localizing 3H-GABA in nerve terminals of rat cerebral cortex by electron microscopic autoradiography. Nature 229, 628–630.CrossRefGoogle Scholar
  14. Bloomquist, J. R., ffrench-Constant, R. H., and Roush, R. T. (1991) Exitation of central neurons by dieldrin and picrotoxinin in susceptible and resistant Drosophila melanogaster (Meigen). Pestic. Sci. 32, 463–469.CrossRefGoogle Scholar
  15. Bormann, J., Hamill, O. P. and Sakmann, B. (1987) Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones. J. Physiol. 385, 243–286.Google Scholar
  16. Bowery, N. G., Hill, D. R., Hudson, A. L., Doble, A., Middlemiss, D. N., Shaw, J. and Turnbull, M. (1980) (—)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature 283, 92–94.Google Scholar
  17. Braestrup, C. and Squires, R. F. (1977) Specific benzodiazepine receptors in rat brain characterized by high affinity [3H] diazepam binding. Proc. Natl. Acad. Sci. USA 74, 3805–3809.CrossRefGoogle Scholar
  18. Braestrup, C., Nielsen, M. and Olsen, C. E. (1980) Urinary and brain β-carboline-3-carboxylates as potent inhibitors of brain benzodiazepine receptors. Proc. Natl. Acad. Sci. USA 77, 2288–2292.CrossRefGoogle Scholar
  19. Brattsten, L. B., Holyoke, C. W., Leeper, J. R. and Raffa, K. F. (1986) Insecticide resistance: challenge to pest management and basic research. Science 231, 1255–1260.CrossRefGoogle Scholar
  20. Breer, H. and Heilgenberg, H. (1985) Neurochemistry of GABAergic activities in the central nervous system of Locusta migratoria. J. Comp. Physiol. A 157, 343–354.CrossRefGoogle Scholar
  21. Brennan, M. J. W. (1982) GABA autoreceptors are not coupled to benzodiazepine receptors in rat cerebral cortex. J. Neurochem. 38, 264–266.CrossRefGoogle Scholar
  22. Brooks, G. T. and Mace, D. W. (1987) Toxicity and mode of action of reductively dechlorinated cyclodiene insecticide analogues on houseflies (Musca domestica L.) and other Diptera. Pestic. Sci. 21, 129–142.CrossRefGoogle Scholar
  23. Brown, M. C. S., Lunt, G. G. and Stapleton, A. (1989) Further characterization of the [35S]-TBPS binding site of the GABA receptor complex in locust (Schistocerca gregaria) ganglia membranes. Comp. Biochem. Physiol. 92C, 9–13.Google Scholar
  24. Browner, M., Ferkany, J. W. and Enna, S. J. (1981) Biochemical identification of pharmacologically and functionally distinct GABA receptors in rat brain. J. Neurosci. 1, 514–518.Google Scholar
  25. Burch, T. P., Thyagarajan, R. and Ticku, M. K. (1983) Group-selective modification of the benzodiazepine-γ-aminobutyric acid receptor-ionophore complex reveals that low-affinity γ-aminobutyric acid receptors stimulate benzodiazepine binding. Mol. Pharmacol. 23, 52–59.Google Scholar
  26. Callachan, H., Cottrell, G. A., Hather, N. Y., Lambert, J. J., Nooney, J. M. and Peters, J. A. (1987) Modulation of the GABAA receptor by progesterone metabolites. Proc. R. Soc. Lond. B 231, 359–369.CrossRefGoogle Scholar
  27. Casalotti, S. O., Stephenson, F. A. and Barnard, E. A. (1986) Separate subunits for agonist and benzodiazepine binding in the γ-aminobutyric acidA receptor oligomer. J. Biol. Chem. 261, 15013–15016.Google Scholar
  28. Casida, J. E. and Lawrence, L. J. (1985) Structure-activity correlations for interactions of bicyclophosphorus esters and some polychlorocycloalkane and pyrethroid insecticides with the brain specific t-butylbicyclophosphorothionate receptor. Environ. Health Perspect. 61, 123–132.CrossRefGoogle Scholar
  29. Casida, J. E., Palmer, C. J. and Cole, L. M. (1985) Bicycloorthocarboxylate convulsants - Potent GABAA receptor antagonists. Mol. Pharmacol. 28, 246–253.Google Scholar
  30. Casida, J. E., Nicholson, R. A. and Palmer, C. J. (1988) Trioxabicyclooctanes as probes for the convulsant site of the GABA-gated chloride channel in mammals and arthropods, in: Neurotox88: Molecular Basis of Drug and Pesticide Action, pp. 125–144. Ed. G. G. Lunt. Elsevier Science Publishers BV (Biomedical Division), Amsterdam.Google Scholar
  31. Changeux, J.-P., Giraudet, J. and Dennis, M. (1987) The nicotinic acetylcholine receptor: molecular architecture of a ligand-regulated ion channel. TIBS 8, 459–465.Google Scholar
  32. Cohen, E. and Casida, J. E. (1985) Chlorocyelohexane insecticides and male medfly attractants: similar stereospecificity for neuroactivity and interactions with a housefly [35S]t-butylbicyclophosphorothionate binding site. Life Sci. 36, 1837–1842.CrossRefGoogle Scholar
  33. Cohen, E. and Casida, J. E. (1986) Effects of insecticides and GABAergic agents on a housefly [35S]t-butylbicyclophosphorothionate binding site. Pestic. Biochem. Physiol. 25, 63–72.CrossRefGoogle Scholar
  34. Cole, L. M. and Casida, J. E. (1986) Polychlorocycloalkane insecticide-induced convulsions in mice in relation to disruption of the GABA-regulated chlorine ionophore. Life Sci. 39, 1855–1862.CrossRefGoogle Scholar
  35. Cooper, S. J., Kirkham, T. C. and Estall, L. B. (1987) Pyrazoloquinolines: second generation benzodiazepine receptor ligands have heterogenous effects. TIPS 8, 180–184.Google Scholar
  36. Curtis, D. R., Duggan, A. W., Feliz, D. and Johnston, G. A. R. (1970) GABA, bicuculline and central inhibition. Nature 266, 1222–1224.CrossRefGoogle Scholar
  37. Cutting, G. R., Lu, L., O’Hara, B. F., Kasch, L. M., Montrose-Rafizadeh, C., Donovan, D. M., Shimada, S., Antonarakis, S. E., Guggino, W. B., Uhl, G. R. and Kazazian, H. H. (1991) Cloning of the γ-aminobutyric acid (GABA) ρ1 cDNA: A GABA receptor subunit highly expressed in the retina. Proc. Natl. Acad. Sci. USA 88, 2673–2677.CrossRefGoogle Scholar
  38. David, J. A. and Sattelle, D. B. (1984) Actions of cholinergic pharmacological agents on the cell body membrane of the fast coxal depressor motoneurone of the cockroach (Periplaneta americana). J. Exp. Biol. 108, 119–136.Google Scholar
  39. Deng, L., Ransom, R. W. and Olsen, R. W. (1986) [3H]Muscimol photolabels the γ-aminobutyric acid receptor binding site on a peptide subunit distinct from that labeled with benzodiazepines. Biochem. Biophys. Res. Commun. 138, 1308–1314.Google Scholar
  40. Deng, L., Palmer, C. J. and Casida, J. E. (1991) House fly brain γ-aminobutyric acid-gated chloride channel: Target for multiple classes of insecticides. Pestic. Biochem. Physiol. 41, 60–65.CrossRefGoogle Scholar
  41. Doble, A. and Martin, I. L. (1992) Multiple benzodiazepine receptors: no reasons for anxiety. TIPS 13, 76–81.Google Scholar
  42. Duce, I. R. and Scott, R. H. (1983) GABA sensitivity in the distal bundles of the locust extensor tibiae muscle. J. Physiol. 343, 31–32 P.Google Scholar
  43. Duman, R. S., Sweetnam, P. ML, Gallombardo, P. A. and Tallman, J. F. (1987) Molecular biology of inhibitory amino acid receptors. Mol. Neurobiol. 1, 155–189.CrossRefGoogle Scholar
  44. Eto, M., Ozoe, Y., Fujita, T. and Casida, J. E. (1976) Significance of branched bridge-head substituent in toxicity of bicyclic phosphate esters. Agr. Biol. Chem. 40, 2113–2115.CrossRefGoogle Scholar
  45. ffrench-Constant, R. H., Mortlock, D. P., Shaffer, C. D., Maclntyre, R. J. and Roush, R. T. (1991) Molecular cloning and transformation of cyclodiene resistance in Drosophila: An invertebrate γ-aminobutyric acid subtype A receptor locus. Proc. Natl. Acad. Sci. USA 88, 7209–7213.CrossRefGoogle Scholar
  46. Foster, G. G., Whitten, M. J., Konovalov, C, Arnold, J. T. A. and Maffi, G. (1981) Autosomal genetic maps of the Australian sheep blowfly Lucilia cuprina dorsalis R.-D. (Diptera: Calliphoridae), and possible correlations with the linkage maps of Musca domestica L. and Drosophila melanogaster (Mg.) Genet. Res. 37, 55–69.CrossRefGoogle Scholar
  47. Fraser, C. M. (1990) Expression of receptor genes in cultured cells, in: Receptor Biochemistry: A Practical Approach, pp. 263–275. ED. E. C. Hulme. Oxford University Press.Google Scholar
  48. Gahwiler, B. H., Maurer, R. and Wuthrich, H. J. (1984) Pitrazepin: a novel GABAA antagonist. Neurosci. Lett. 45, 311–316.CrossRefGoogle Scholar
  49. Gallagher, J. P., Higashi, H. and Nishi, S. (1978) Characterization and ionic basis of GABA-induced depolarizations recorded in vitro from cat primary afferent neurones. J. Physiol. 275, 263–282.Google Scholar
  50. Gant, D. B., Eldefrawi, M. E. and Eldefrawi, A. T. (1987) Cyclodiene insecticides inhibit GABAA receptor regulated-chloride transport. Toxicol. Appl. Pharmacol. 88, 313–321.CrossRefGoogle Scholar
  51. Gant, D. B., Bloomquist, J. R., Ayad, H. M. and Chalmers, A. E. (1990) A comparison of mammalian and insect GABA receptor chloride channels. Pestic. Sci. 30, 355–357.Google Scholar
  52. Georghiou, G. P. and Mellon, R. (1983) Pesticide resistance in time and space, in: Pest Resistance to Pesticides, pp. 1–46. Eds G. P. Georghiou and T. Saito. Plenum, New York.Google Scholar
  53. Gerschenfeld, H. M. (1973) Chemical transmission in invertebrate central nervous system and neuromuscular junctions. Physiol. Rev. 53, 1–119.Google Scholar
  54. Ghiasuddin, S. M. and Matsumura, F. (1982) Inhibition of gamma-aminobutyric acid (GABA)-induced chloride uptake by gamma-BHC and heptachlor epoxide. Comp. Biochem. Physiol. 73C, 141–144.Google Scholar
  55. Giles, D. and Usherwood, P. N. R. (1985) The effects of putative amino acid neurotransmitters on somata isolated from neurons of the locust central nervous system. Comp. Biochem. Physiol. 80C, 231–236.CrossRefGoogle Scholar
  56. Greenlee, D. V., Van Ness, P. C. and Olsen, R. W. (1978) Gamma-aminobutyric acid binding in mammalian brain: receptor-like specificity of sodium-independent sites. J. Neurochem. 31, 933–938.CrossRefGoogle Scholar
  57. Grenningloh, G., Rientz, A., Schmitt, B., Methfessel, C., Zensen, M., Beyreuther, K., Gundelfinger, E. D. and Betz, H. (1987a) The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328, 215–220.CrossRefGoogle Scholar
  58. Grenningloh, G., Gundelfinger, E. D., Schmitt, B. and Betz, H. (1987b) Glycine vs GABA receptors. Nature 330, 25.CrossRefGoogle Scholar
  59. Guidotti, A., Gale, K., Suria, A. and Toffano, G. (1979) Biochemical evidence for two classes of GABA receptors in rat brain. Brain Res. 172, 566–571.CrossRefGoogle Scholar
  60. Haefely, W. (1991) Comparative pharmacology of benzodiazepine receptor ligands with differing intrinsic efficacy, in: Transmitter Amino Acid Receptors: Structures, Transduction and Models for Drug Development, pp. 91–111. Eds E. A. Barnard and E. Costa. Fidia Research Foundation Symposium Series 6, Thieme Medical Publishers, New York.Google Scholar
  61. Harris, R. A. and Allan, A. M. (1985) Functional coupling of 7-aminobutyric acid receptors to chloride channels in brain membranes. Science 228, 1108–1110.CrossRefGoogle Scholar
  62. Harrison, N. L., Majewska, M. D., Harrington, J. W. and Barker, J. L. (1987) Structure-activity relationships for steroid interaction with the γ-aminobutyric acidA receptor complex. J. Pharmacol Exp. Ther. 241, 346–353.Google Scholar
  63. Harvey, R. J., Vreugdenhil, E., Zaman, S. H., Bhandal, N. S., Usherwood, P. N. R., Barnard, E. A. and Darlison, M. G. (1991) Sequence of a functional invertebrate GABAA receptor subunit which can form a chimaeric receptor with a vertebrate α subunit. EM BO J. 10, 3239–3245.Google Scholar
  64. Havoundjian, H., Paul, S. M. and Skolnick, P. (1986) The permeability of γ-aminobutyric acid-gated chloride channels is described by the binding of a “cage” convulsant, i-butylbicyclophosphoro[35S]thionate. Proc. Natl. Acad. Sci. USA 83, 9241–9244.CrossRefGoogle Scholar
  65. Hill, D. R. (1985) GABAB receptor modulation of adenylate cyclase activity in rat brain slices. Br. J. Pharmacol. 84, 249–257.Google Scholar
  66. Holland, K. D., McKeon, A. C., Covey, D. F. and Ferrendelli, J. A. (1990a) Binding interactions of convulsant and anticonvulsant γ-butyrolactones and γ-thiobutyrolactones with the picrotoxin receptor. J. Pharmacol. Exp. Therap. 254, 578–583.Google Scholar
  67. Holland, K. D., Ferrendelli, J. A., Covey, D. F. and Rothman, S. M. (1990b) Physiological regulation of the picrotoxin receptor by γ-butyrolactones and γ-thiobutyrolactones in cultured hippocampal neurones. J. Neurosci. 10, 1719–1727.Google Scholar
  68. Holz, G. G., Rane, S. G. and Dunlap, K. (1986) GTP-binding proteins mediate transmitter inhibitions of voltage-dependent calcium channels. Nature 319, 670–672.CrossRefGoogle Scholar
  69. Homma, S. and Rovainen, C. M. (1978) Conductance increases produced by glycine and γ-aminobutyric acid in lamprey interneurones. J. Physiol. 279, 231–252.Google Scholar
  70. Hue, B. (1991) Functional assay for GABA receptor subtypes of a cockroach giant interneuron. Arch. Insect Biochem. Physiol. 18, 147–157.CrossRefGoogle Scholar
  71. Hunkeler, W., Mohler, H., Pieri, L., Polc, P., Bonetti, E. P., Cumin, R., Schaffner, R. and Haefely, W. (1981) Selective antagonists of benzodiazepines. Nature 290, 514–516.CrossRefGoogle Scholar
  72. Inoue, M., Matsuo, T. and Ogata, N. (1985) Possible involvement of K+-conductance in the action of γ-aminobutyric acid in the guinea-pig hippocampus. Br. J. Pharmacol. 86, 515–524.Google Scholar
  73. Johnston, G. A. R. and Willow, M. (1982) GABA and barbiturate receptors. TIPS 3, 328–330.Google Scholar
  74. Kadous, A. A., Ghiasuddin, S. M., Matsumura, F., Scott, J. G. and Tanaka, K. (1983) Difference in the picrotoxinin receptor between the cyclodiene-resistant and susceptible strains of the German cockroach. Pestic. Biochem. Physiol. 19, 157–166.CrossRefGoogle Scholar
  75. Karbon, E. W. and Enna, S. J. (1985) Characterization of the relationship between γ-aminobutyric acid B agonists and transmitter-coupled cyclic nucleotide-generating systems in rat brain. Mol. Pharmacol. 27, 53–59.Google Scholar
  76. Karobath, M. and Sperk, G. (1979) Stimulation of benzodiazepine receptor binding by gamma-aminobutyric acid. Proc. Natl. Acad. Sci. USA 76, 1004–1006.CrossRefGoogle Scholar
  77. Kerkut, G. A., Pitman, R. M. and Walker, R. J. (1969) Sensitivity of neurones of the insect central nervous system to ionophoretically applied acetylcholine or GABA. Nature 222, 1075–1076.CrossRefGoogle Scholar
  78. Kirkness, E. F. and Turner, A. J. (1988) Antibodies directed against a nonapeptide sequence of the γ-aminobutyrate (GABA)/benzodiazepine receptor α-subunit. Biochem. J. 256, 291–294.Google Scholar
  79. Kleingoor, C., Ewert, M., von Blankenfeld, G., Seeburg, P. H. and Kettenmann, H. (1991) Inverse but not full benzodiazepine agonists modulate recombinant α6β2γ2GABAA receptors in transfected human embryonic kidney cells. Neurosci. Letts. 130, 169–172.CrossRefGoogle Scholar
  80. Klunk, W. E., Covey, D. F. and Ferrendelli, J. A. (1982a) Comparison of epileptogenic properties of unsubstituted and β-alkyl substituted γ-butyrolactones. Mol. Pharmacol. 22, 431–437.Google Scholar
  81. Klunk, W. E., Covey, D. F. and Ferrendelli, J. A. (1982b) Anticonvulsant properties of α-, γ- and α, γ-substituted γ-butyrolactones. Mol. Pharmacol. 22, 438–443.Google Scholar
  82. Klunk, W. E., Kalman, B. L., Ferrendelli, J. A. and Covey, D. F. (1983) Computer-assisted modeling of the picrotoxinin and γ-butyrolactone receptor site. Mol. Pharmacol. 23, 511–518.Google Scholar
  83. Krespan, B., Springfield, S. A., Haas, H. and Geller, H. M. (1984) Electrophysiological studies on benzodiazepine antagonists. Brain Res. 295, 265–274.CrossRefGoogle Scholar
  84. Krogsgaard-Larsen, P., Hjeds, H., Curtis, D. R., Lodge, D. and Johnston, G. A. R. (1979) Dihydromuscimol, thiomuscimol and related heterocyclic compounds as GABA analogues. J. Neurochem. 32, 1717–1724.CrossRefGoogle Scholar
  85. Krogsgaard-Larsen, P. and Falch, E. (1981) GAB A agonists: development and interactions with the GABA receptor complex. Mol. Cell. Biochem. 38, 129–146.CrossRefGoogle Scholar
  86. Krnjevic, K. and Schwartz, S. (1966) Is γ-aminobutyric acid an inhibitory neurotransmitter? Nature 211, 1372–1374.CrossRefGoogle Scholar
  87. Krnjevic, K. (1974) Chemical nature of synaptic transmission in vertebrates. Physiol. Rev. 54, 418–540.Google Scholar
  88. Lawrence, L. J. and Casida, J. E. (1984) Interactions of lindane, toxaphene and cyclodienes with brain-specific t-butylbicyclophosphorothionate receptor. Life Sci. 35, 171–178.CrossRefGoogle Scholar
  89. Leeb-Lundberg, F., Snowman, A. and Olsen, R. W. (1980) Barbiturate receptor sites are coupled to benzodiazepine receptors. Proc. Natl. Acad. Sci. USA 77, 7468–7472.CrossRefGoogle Scholar
  90. Lees, G., Beadle, D. J., Neumann, R. and Benson, J. A. (1987) Responses to GABA by isolated insect neuronal somata: pharmacology and modulation by a benzodiazepine and a barbiturate. Brain Res. 401, 267–278.CrossRefGoogle Scholar
  91. Levitan, E. S., Schofield, P. R., Burt, D. R., Rhee, L. M., Wisden, W., Kohler, M., Fujita, N., Rodriguez, H. F., Stephenson, F. A., Darlison, M. G., Barnard, E. A. and Seeburg, P. H. (1988) Structural and functional basis for GABAA receptor heterogenity. Nature 335, 76–79.CrossRefGoogle Scholar
  92. Luddens, H., Pritchett, D. B., Kohler, M., Killisch, I., Keinanen, K., Monyer, H., Sprengel, R. and Seeburg, P. H. (1990) Cerebellar GABAA receptor selective for a behavioural alcohol antagonist. Nature 346, 648–651.CrossRefGoogle Scholar
  93. Lummis, S. C. R. and Sattelle, D. B. (1986) Binding sites for [3H]GABA, [3H]flunitrazepam and [35S]TBPS in insect CNS. Neurochem. Int. 9, 287–293.CrossRefGoogle Scholar
  94. Lummis, S. C. R. (1990) GABA receptors in insects. Comp. Biochem. Physiol. 95C, 1–8.Google Scholar
  95. Lummis, S. C. R., Buckingham, S. D., Rauh, J. J. and Sattelle, D. B. (1990) Blocking actions of heptachlor at an insect central nervous system GABA receptor. Proc. R. Soc. Lond. B 240, 97–106.CrossRefGoogle Scholar
  96. Lunt, G. G., Robinson, T. N., Miller, T., Knowles, W. P. and Olsen, R. W. (1985) The identification of GABA receptor binding sites in insect ganglia. Neurochem. Int. 7, 751–754.CrossRefGoogle Scholar
  97. Macksay, G. and Ticku, M. K. (1985) Dissociation of [35S]t-butylbicyclophosphorothionate binding differentiates convulsant and depressant drugs that modulate GABAergic transmission. J. Neurochem. 44, 480–486.CrossRefGoogle Scholar
  98. Majewska, M. D., Harrison, N. L., Schwartz, R. D., Barker, J. L. and Paul, S. M. (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232, 1004–1007.CrossRefGoogle Scholar
  99. Malecot, C. O. and Sattelle, D. B. (1990) Single channel recordings from insect neuronal GABA-activated chloride channels. J. Exp. Biol. 151, 495–501.Google Scholar
  100. Mamalaki, C., Stephenson, F. A. and Barnard, E. A. (1987) The GABA/benzodiazepine receptor is a heterotetramer of homologous α and β subunits. EM BO J. 6, 561–565.Google Scholar
  101. Mamalaki, C., Barnard, E. A. and Stephenson, F. A. (1989) Molecular size of the γ-aminobutyric acid receptor purified from mammalian cerebral cortex. J. Neurochem. 52, 124–134.CrossRefGoogle Scholar
  102. Marangos, P. J., Patel, J., Boulenger, J.-P. and Clark-Rosenberg, R. (1982) Characterization of peripheral-type benzodiazepine binding sites in brain using [3H]Ro5-4864. Mol. Pharmacol. 22, 26–32.Google Scholar
  103. Matsumura, F. and Ghiasuddin, S. M. (1983) Evidence for similarities between cyclodiene type insecticides and picrotoxinin in their action mechanisms. J. Environ. Sci. Health B 18 1–14.CrossRefGoogle Scholar
  104. Matsumura, F., Tanaka, K. and Ozoe, Y. (1987) GABA related systems as targets for insecticides, in: Sites of Action for Neurotoxic Pesticides, pp. 44–70. Eds R. M. Hollingworth and M. B. Green. American Chemical Society Symposium Society, American Chemical Society, Washington, D.C.CrossRefGoogle Scholar
  105. McKernan, R. M., Quiek, K., Prince, R., Cox, P. A., Gillard, N. P., Ragan, C. I. and Whiting, P. (1991) GABAA receptor subtypes immunopurified from rat brain with α subunit-specific antibodies have unique pharmacological properties. Neuron 7, 667–676.CrossRefGoogle Scholar
  106. Mohler, H., Sigel, E., Malherbe, P., Richards, J. G., Persohn, E., Mertens, S. and Benke, D. (1991) Gamma-aminobutyric acid (GABA)A-receptor heterogeneity: Functional architecture of receptors and sites of subunit-expression, in: Transmitter Amino Acid Receptors: Structures, Transduction and Models for Drug Development, pp. 23–35. Eds E. A. Barnard and E. Costa. Fidia Research Foundation Symposium Series 6. Thieme Medical Publishers, New York.Google Scholar
  107. Moss, S. J., Smart, T. G., Porter, N. M., Nayeem, N., Devine, J., Stephenson, F. A., Macdonald, R. L. and Barnard, E. A. (1990) Cloned GABA receptors are maintained in a stable cell line: allosteric and channel properties. Eur. J. Pharmacol. (Mol. Pharmacol.) 189, 77–88.CrossRefGoogle Scholar
  108. Murphy, V. F. and Wann, K. T. (1988) The action of GABA receptor agonists and antagonists on muscle membrane conductance in Schistocerca gregaria. Br. J. Pharmacol. 95, 713–722.Google Scholar
  109. Nielsen, M., Gredal, O. and Braestrup, C. (1979) Some properties of 3H-diazepam displacing activity from human urine. Life Sci. 25, 679–686.CrossRefGoogle Scholar
  110. Nielsen, M., Schou, H. and Braestrup, C. (1981) [3H]Propyl β-carboline-3-carboxylate binds specifically to brain benzodiazepine receptors. J. Neurochem. 36, 276–285.CrossRefGoogle Scholar
  111. Obata, K., Takeda, K. and Shinozaki, H. (1970) Further study on the pharmacological properties of the cerebellar induced inhibition of Deiter’s neurones. Exp. Brain. Res. 11, 327–342.CrossRefGoogle Scholar
  112. Obata, T., Yamamura, H. I., Malatynska, E., Ikeda, M., Laird, H., Palmer, C. J. and Casida, J. E. (1988) Modulation of γ-aminobutyric acid-stimulated chloride influx by bicycloorthocarboxylates, bicyclophosphorus esters, polychlorocycloalkanes and other cage convulsants. J. Pharmacol. Exp. Ther. 244, 802–806.Google Scholar
  113. Olsen, R. W., Ticku, M. K. and Miller, T. (1978) Dihydropicrotoxinin binding to crayfish muscle sites possibly related to γ-aminobutyric acid receptor-ionophores. Mol. Pharmacol. 14, 381–391.Google Scholar
  114. Olsen, R. W. (1981) GABA-benzodiazepine-barbiturate receptor interactions. J. Neurochem. 37, 1–13.CrossRefGoogle Scholar
  115. Olsen, R. W. and Snowman, A. M. (1982) Chloride-dependent enhancement by barbiturates of γ-aminobutyric acid receptor binding. J. Neurosci. 2, 1812–1823.Google Scholar
  116. Olsen, R. W. and Snowman, A. M. (1983) [3H]Bicuculline methochloride binding to low-affinity γ-aminobutyric acid receptor sites. J. Neurochem. 41, 1653–1663.CrossRefGoogle Scholar
  117. Olsen, R. W. and Venter, J. C. (1986) (Eds) in: Benzodiazepine/GABA Receptors and Chloride Channels: Structural and Functional Properties. Alan R. Liss, New York.Google Scholar
  118. Olsen, R. W., Szamraj, O. and Miller, T. (1989) [35S]t-Butylbicyclophosphorothionate binding sites in invertebrate tissues. J. Neurochem. 52, 1311–1318.CrossRefGoogle Scholar
  119. Olsen, R. W. and Tobin, A. J. (1990) Molecular biology of GABAA receptors. FASEB J. 4, 1469–1480.Google Scholar
  120. Ong, J. and Kerr, D. I. B. (1990) GABA-receptors in peripheral tissues. Life Sci. 46, 1489–1501.CrossRefGoogle Scholar
  121. Oppenoorth, F. J. and Nasrat, G. E. (1966) Genetics of dieldrin and γ-BHC resistance in the housefly. Ent. Exp. Appl. 9, 223–231.CrossRefGoogle Scholar
  122. Oppenoorth, F. J. (1985) Biochemistry and genetics of insecticide resistance, in: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 12, pp. 731–773. Eds G. A. Kerkut and L. I. Gilbert. Pergamon Press, Oxford.Google Scholar
  123. Ozoe, Y. and Matsumura, F. (1986) Structural requirements for bridged bicyclic compounds acting on picrotoxinin receptor. J. Agric. Food Chem. 34, 126–134.CrossRefGoogle Scholar
  124. Ozoe, Y., Mochida, K., Nakamura, T., Yoyama, A. and Matsumura, F. (1987) Actions of benzodiazepines on the housefly: binding to thorax/abdomen extracts and biological effects. Comp. Biochem. Physiol. 87C, 187–191.CrossRefGoogle Scholar
  125. Ozoe, Y., Fukuda, K., Mochida, K. and Nakamura, T. (1989) Actions of benzodiazepines on the housefly. 3. In vitro binding of [3H]Ro5-4864 responding to GABA receptor ligands. Comp. Bichem. Physiol. 93C, 193–199.CrossRefGoogle Scholar
  126. Papazian, D. M., Schwarz, T. L., Tempel, B. L., Jan, Y. N. and Jan, L. Y. (1987) Cloning of genomic and complementary DNA from shaker, a putative potassium channel gene from Drosophila. Science 237, 749–753.CrossRefGoogle Scholar
  127. Pinnock, R. D., David, J. A. and Sattelle, D. B. (1988) Ionic events following GABA receptor activation in an identified insect motor neuron. Proc. R. Soc. Lond. B 232, 457–470.CrossRefGoogle Scholar
  128. Pitman, R. M. and Kerkut, G. A. (1970) Comparison of the actions of ionophoretically applied acetylcholine and gamma aminobutyric acid with the EPSP and IPSP in cockroach central neurons. Comp. Gen. Pharmacol. 1, 221–230.CrossRefGoogle Scholar
  129. Pole, P., Ropert, N. and Wright, D. M. (1981) Ethyl β-carboline-3-carboxylate antagonizes the action of GABA and benzodiazepines in the hippocampus. Brain Res. 217, 216–220.CrossRefGoogle Scholar
  130. Pritchett, D. B., Sontheimer, H., Gorman, C. M., Kettenmann, H., Seeburg, P. H. and Schofield, P. R. (1988) Transient expression shows ligand gating and allosteric potentiation of GABAA receptor subunits. Science 242, 1306–1308.CrossRefGoogle Scholar
  131. Pritchett, D. B., Sontheimer, H., Shivers, B. D., Ymer, S., Kettenmann, H., Schofield, P. R. and Seeburg, P. H. (1989a) Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338, 582–585.CrossRefGoogle Scholar
  132. Pritchett, D. B., Luddens, H. and Seeburg, P. H. (1989b) Type I and Type II GABAA-benzodiazepine receptors produced in transfected cells. Science 245, 1389–1392.CrossRefGoogle Scholar
  133. Pritchett, D. B. and Seeburg, P. H. (1990) γ-Aminobutyric acidA receptor α5-subunit creates novel type II benzodiazepine receptor pharmacology. J. Neurochem. 54, 1802–1804.CrossRefGoogle Scholar
  134. Pritchett, D. B. and Seeburg, P. H. (1991) γ-Aminobutyric acid type A receptor point mutation increases the affinity of compounds for the benzodiazepine site. Proc. Natl. Acad. Sci. USA 88, 1421–1425.CrossRefGoogle Scholar
  135. Puia, G., Vicini, S., Seeburg, P. H. and Costa, E. (1991) Influence of recombinant γ-aminobutyric acid-A receptor subunit composition on the action of allosteric modulators of γ-aminobutyric acid-gated Cl- currents. Mol. Pharmacol. 39, 691–696.Google Scholar
  136. Ramanjaneyulu, R. and Ticku, M. K. (1983) Differential interactions of depressant and convulsant drugs with the components of the benzodiazepine-GABA receptor-ionophore complex. Neurosci. Abs. 9, 403.Google Scholar
  137. Ramanjaneyulu, R. and Ticku, M. K. (1984) Binding characteristics and interactions of depressant drugs with [35S]t-butylbicyclophosphorothionate, a ligand that binds to the picrotoxinin site. J. Neurochem. 42, 221–229.CrossRefGoogle Scholar
  138. Rauh, J. J., Lummis, S. C. R. and Sattelle, D. B. (1990) Pharmacological and biochemical properties of insect GABA receptors. TIPS 11, 325–329.Google Scholar
  139. Regan, J. W., Yamamura, H. I., Yamada, S. and Roeske, W. R. (1981) High affinity renal [3H]flunitrazepam binding: characterization, localization and alteration in hypertension. Life Sci. 28, 991–997.CrossRefGoogle Scholar
  140. Robinson, T., MacAllan, D., Lunt, G. G. and Battersby, M. (1986) γ-Aminobutyric acid receptor complex of insect CNS: characterization of a benzodiazepine binding site. J. Neurochem. 47, 1955–1962.CrossRefGoogle Scholar
  141. Rutherford, D. M., Jeffrey, D., Lunt, G. G. and Weitzman, P. D. J. (1987) GABA binding to receptor sites in locust supraoesophageal ganglia. Neurosci. Lett. 79, 337–340.CrossRefGoogle Scholar
  142. Sattelle, D. B., Pinnock, R. D., Wafford, K. A. and David, J. A. (1988a) GABA receptors on the cell body membrane of an identified insect motor neuron. Proc. R. Soc. Lond. B 232, 443–456.CrossRefGoogle Scholar
  143. Sattelle, D. B., Leech, C. A., Lummis, S. C. R., Harrison, B. J., Robinson, H. P. C., Moores, G. D. and Devonshire, A. L. (1988b) Ion channel properties of insects susceptible and resistant to insecticides, in: Neurotox88: Molecular Basis of Drug and Pesticide Action, pp. 563–582. Ed. G. G. Lunt. Elsevier Science Publishers BV.Google Scholar
  144. Sattelle, D. B. (1990) GABA receptors of insects. Adv. Insect Physiol. 22, 1–113.CrossRefGoogle Scholar
  145. Sattelle, D. B., Lummis, S. C. R., Wong, J. F. H. and Rauh, J. J. (1991a) Pharmacology of insect GABA receptors. Neurochem. Res. 16, 363–374.CrossRefGoogle Scholar
  146. Sattelle, D. B., Marshall, J., Lummis, S. C. R., Leech, C. A., Miller, K. W. P., Anthony, N. M., Bai, D., Wafford, K. A., Harrison, J. B., Chapaitis, L. A., Watson, M. K., Benner, E. A., Vassallo, J. G., Wong, J. F. H. and Rauh, J. J. (1991b) γ-Aminobutyric acid and L-glutamate receptors of insect nervous tissue, in: Transmitter Amino Acid Receptors: Structures, Transduction and Models for Drug Development, pp. 273–291. Eds E. A. Barnard and E. Costa. Fidia Research Foundation Symposium Series 6. Thieme Medical Publishers, New York.Google Scholar
  147. Schoemaker, H., Bliss, M. and Yamamura, H. I. (1981) Specific high affinity saturable binding of [3H]Ro5-4864 to benzodiazepine binding sites in the rat cerebral cortex. Eur. J. Pharmacol. 71, 173–175.CrossRefGoogle Scholar
  148. Schofield, P. R., Darlison, M. G., Fujita, N., Burt, D. R., Stephenson, F. A., Rodriguez, H., Rhee, L. M., Ramachandran, J., Reale, V., Glencorse, T. A., Seeburg, P. H. and Barnard, E. A. (1987) Sequence and expression of the GABAA receptor shows a ligand-gated receptor super-family. Nature 328, 221–227.CrossRefGoogle Scholar
  149. Schofield, P. R., Pritchett, D. B., Sontheimer, H., Ketenmann, H. and Seeburg, P. H. (1989) Sequence and functional expression of human GABAA receptor α1, and β subunits. FEBS Lett. 244, 361–364.CrossRefGoogle Scholar
  150. Scott, R. H. and Duce, I. R. (1987a) Inhibition and gamma-aminobutyric acid-induced conductance on locust (Schistocerca gregaria) extensor tibiae muscle fibres. J. Insect Physiol. 33, 183–189.CrossRefGoogle Scholar
  151. Scott, R. H. and Duce, I. R. (1987b) Pharmacology of GABA receptors on skeletal muscle fibres of the locust (Schistocerca gregaria). Comp. Biochem. Physiol. 86C, 305–311.CrossRefGoogle Scholar
  152. Seeburg, P. H., Widen, W., Verdoorn, T. A., Pritchett, D. B., Werner, P., Herb, A., Luddens, H., Sprengel, R. and Sakmann, B. (1990) The GABAA receptor family: molecular functional diversity. Cold Spring Harbor Symposia on Quantitative Biology LV, 29–40.Google Scholar
  153. Seeburg, P. H., Wisden, W., Pritchett, D. B., Wieland, H. and Luddens, H. (1991) (Gamma-aminobutyric acid)A benzodiazepine receptors in the brain: from subunit to subtype, in: Transmitter Amino Acid Receptors: Structures, Tranduction and Models for Drug Development, pp. 13–22. Eds E. A. Barnard and E. Costa. Fidia Research Foundation Symposium Series 6. Thieme Medical Publishers, New York.Google Scholar
  154. Shankland, D. L. and Schroeder, M. E. (1973) Pharmacological evidence for a discrete neurotoxic action of dieldrin (HEOD) in the American cockroach, Periplaneta americana (L.). Pestic. Biochem. Physiol. 3, 77–86.CrossRefGoogle Scholar
  155. Shimahara, T., Pichon, Y., Lees, G., Beadle, C. A. and Beadle, D. J. (1987) Gamma-aminobutyric acid receptors on cultured cockroach brain neurones. J. Exp. Biol. 131, 231–244.Google Scholar
  156. Siegfried, B. D. and Mullin, C. A. (1990) Metabolism, penetration and partitioning of [14C]-aldrin in aldrin resistant and susceptible corn rootworms. Pestic. Biochem. Physiol. 36, 135–146.CrossRefGoogle Scholar
  157. Sigel, E., Stephenson, F. A., Mamalaki, C. and Barnard, E. A. (1983) A γ-aminobutyric acid/benzodiazepine receptor complex of bovine cerebral cortex. J. Biol. Chem. 258, 6965–6971.Google Scholar
  158. Sigel, E., Baur, R., Trube, G., Mohler, H. and Malherbe, P. (1990) The effect of subunit composition of rat brain GABAA receptors on channel function. Neuron 5, 703–711.CrossRefGoogle Scholar
  159. Simmonds, M. A. (1980) Evidence that bicuculline and picrotoxin act at separate sites to antagonize γ-aminobutyric acid in rat cuneate nucleus. Neuropharmacology 19, 39–45.CrossRefGoogle Scholar
  160. Simmonds, M. A. (1982) Classification of some GABA antagonists with regard to site of action and potency in slices of rat cuneate nucleus. Eur. J. Pharmacol. 80, 347–358.CrossRefGoogle Scholar
  161. Simmonds, M. A. (1983) Multiple GABA receptors and associated regulatory sites. TINS 6, 279–281.Google Scholar
  162. Simmonds, M. A. and Turner, J. P. (1985) Antagonism of inhibitory amino acids by the steroid derivative RU5135. Br. J. Pharmacol. 84, 631–635.Google Scholar
  163. Simmonds, M. A. (1991) Modulation of the GABAA receptor by steroids. Seminars in the Neurosciences: GABA and inhibitory synaptic transmission 3, 231–239.Google Scholar
  164. Snutch, T. P. (1988) The use of Xenopus oocytes to probe synaptic communication. TINS 11, 250–256.Google Scholar
  165. Soloway, S. B. (1965) Correlation between biological activity and molecular structure of the cyclodiene insecticides. Adv. Pest. Control Res. 6, 85–126.Google Scholar
  166. Squires, R. F., Casida, J. E., Richardson, M. and Saederup, E. (1983) [35S]t-Butylbicyclophosphorothionate binds with high affinity to brain-specific sites coupled to γ-aminobutyric acid-A and ion recognition sites. Mol. Pharmacol. 23, 326–336.Google Scholar
  167. Stephenson, F. A. (1988) Understanding the GABAA receptor: a chemically gated ion channel. Biochem. J. 249, 21–32.Google Scholar
  168. Study, R. E. and Barker, J. L. (1981) Diazepam and (—)-pentobarbital: Fluctuation analysis reveals different mechanisms for potentiation of γ-aminobutyric acid responses in cultured central neurons. Proc. Natl. Acad. Sci. USA 78, 7180–7184.CrossRefGoogle Scholar
  169. Supavilai, P. and Karobath, M. (1984) [35S]-tButylbicyclophosphorothionate binding sites are constituents of the γ-aminobutyric acid benzodiazepine receptor complex. J. Neurosci. 4, 1193–1200.Google Scholar
  170. Taguchi, J. I. and Kuriyama, K. (1984) Purification of γ-aminobutyric acid (GABA) receptor from rat brain by affinity column chromatography using a new benzodiazepine, 1012-S, as an immobilized ligand. Brain Res. 323, 219–226.CrossRefGoogle Scholar
  171. Takeuchi, A. and Takeuchi, N. (1966) A study of the inhibitory action of γ-aminobutyric acid on neuromuscular transmission in the crayfish. J. Physiol. 183, 418–432.Google Scholar
  172. Tallmann, J. F., Thomas, J. W. and Gallager, D. W. (1978) GABAergic modulation of benzodiazepine binding site sensitivity. Nature 274, 383–385.CrossRefGoogle Scholar
  173. Tallman, J. F. and Gallager, D. W. (1985) The GABA-ergic system: A locus of benzodiazepine action. Ann. Rev. Neurosci. 8, 21–44.CrossRefGoogle Scholar
  174. Taniguchi, T., Wang, J. K. T. and Spector, S. (1982) [3H]Diazepam binding sites on rat heart and kidney. Biochem. Pharmacol. 31, 589–590.CrossRefGoogle Scholar
  175. Tanaka, K., Scott, J. G. and Matsumura, F. (1984) Picrotoxin receptor in the central nervous system of the American cockroach: its role in the action of cyclodiene insecticides. Pestic. Biochem. Physiol. 22, 117–127.CrossRefGoogle Scholar
  176. Tenen, S. S. and Hirsch, J. D. (1980) β-Carboline-3-carboxylic acid ethyl ester antagonizes diazepam activity. Nature 288, 609–610.CrossRefGoogle Scholar
  177. Ticku, M. K., Ban, M. and Olsen, R. W. (1978) Binding of [3H]α-dihydropicrotoxinin, a γ-aminobutyric acid synaptic antagonist to rat brain membranes. Mol. Pharmacol. 14, 319–402.Google Scholar
  178. Ticku, M. K. and Macksay, G. (1983) Convulsant/depressant site of action at the allosteric benzodiazepine-GABA receptor ionophore complex. Life Sci. 33, 2363–2375.CrossRefGoogle Scholar
  179. Ticku, M. K. (1986) Convulsant binding sites on the benzodiazepine/GABA receptor, in: Benzodiazepine/GABA Receptors and Chloride Channels: Structural and Functional Properties, pp. 195–207. Eds R. W. Olsen and C. Venter. Alan R. Liss, New York.Google Scholar
  180. Toffano, G., Guidotti, A. and Costa, E. (1978) Purification of an endogenous protein inhibitor of the high affinity binding of γ-aminobutyric acid to synaptic membranes of rat brain. Proc. Natl. Acad. Sci. USA 75, 4024–4028.CrossRefGoogle Scholar
  181. Unwin, N. (1989) The structure of ion channels in membranes of excitable cells. Neuron 3, 665–676.CrossRefGoogle Scholar
  182. Van Renterghem, C., Bilbe, G., Moss, S., Smart, T. G., Constanti, A., Brown, D. A. and Barnard, E. A. (1987) GAB A receptors induced in Xenopus oocytes by chick brain mRNA: evaluation of TBPS as a use-dependent channel-blocker. Mol. Brain. Res. 2, 21–31.CrossRefGoogle Scholar
  183. Vicini, S., Alho, H., Costa, E., Mienville, J.-H, Santi, M. R. and Vaccarino, F. M. (1986) Modulation of γ-aminobutyric acid-mediated inhibitory synaptic currents in dissociated cortical cell cultures. Proc. Natl. Acad. Sci. USA 83, 9269–9273.CrossRefGoogle Scholar
  184. Wafford, K. A. and Sattelle, D. B. (1986) Effects of amino acid neurotransmitter candidates on an identified insect motor neurone. Neurosci. Lett. 63, 135–140.CrossRefGoogle Scholar
  185. Wafford, K. A., Sattelle, D. B., Abalis, I., Eldefrawi, A. T. and Eldefrawi, M. E. (1987) γ-Aminobutyric acid-activated 36C1- influx: A functional in vitro assay for CNS γ- aminobutyric acid receptors of insects. J. Neurochem 48, 177–180.CrossRefGoogle Scholar
  186. Wafford, K. A. and Sattelle, D. B. (1989) L-glutamate receptors on the cell membrane of an identified insect motor neurone. J. Exp. Biol. 144, 449–462.Google Scholar
  187. Wafford, K. A., Lummis, S. C. R. and Sattelle, D. B. (1989a) Block of an insect central nervous system GABA receptor by cyclodiene and cyclohexane insecticides. Proc. R. Soc. Lond. B 237, 53–61.CrossRefGoogle Scholar
  188. Wafford, K. A., Sattelle, D. B., Gant, D. B., Eldefrawi, A. T. and Eldefrawi, M. E. (1989b) Non-competitive inhibition of GABA receptors in insect and vertebrate CNS by endrin and lindane. Pestic. Biochem. Physiol. 33, 213–219.CrossRefGoogle Scholar
  189. Waldrop, B., Christensen, T. A. and Hildebrand, J. G. (1987) GABA-mediated synaptic inhibition of projection neurones in the antennal lobes of the sphinx moth, Manduca sexta. J. Comp. Physiol. A 161, 23–32.CrossRefGoogle Scholar
  190. Walker, R. J. and Holden-Dye, L. (1989) Commentary on the evolution of transmitters, receptors and ion channels in invertebrates. Comp. Biochem. Physiol. 93A, 25–39.CrossRefGoogle Scholar
  191. Weiss, D. S., Barnes, E. M. and Hablitz, J. J. (1988) Whole-cell and single-channel recordings of GABA-gated currents in cultured chick cerebral neurones. J. Neurophysiol. 59, 495–513.Google Scholar
  192. Whiting, P., McKernan, R. M. and Iversen, L. L. (1990) Another mechanism for creating diversity in γ-aminobutyric type A receptors: RNA splicing directs expression of two forms of γ2 subunit, one of which contains a protein kinase C phosphorylation site. Proc. Natl. Acad. Sci. USA 87, 9966–9970.CrossRefGoogle Scholar
  193. Wisden, W., Morris, B. J., Darlison, M. G., Hunt, S. P. and Barnard, E. A. (1988) Distinct GABAA receptor α subunit mRNAs show differential patterns of expression in bovine brain. Neuron 1, 937–947.CrossRefGoogle Scholar
  194. Wisden, W., Morris, B. J., Darlison, M. G., Hunt, S. P. and Barnard, E. A. (1989) Localization of GABAA receptor α-subunit mRNAs in relation to receptor subtypes. Mol. Brain Res. 5, 305–310.CrossRefGoogle Scholar
  195. Wisden, W., Gundlach, A. L., Barnard, E. A., Seeburg, P. H. and Hunt, S. P. (1991) Distribution of GABAA receptor subunit mRNAs in rat lumbar spinal cord. Mol. Brain Res. 10, 179–183.CrossRefGoogle Scholar
  196. Wojcik, W. J. and Neff, N. H. (1984) γ-Aminobutyric acid B receptors are negatively coupled to adenylate cyclase in brain and in the cerebellum these receptors may be associated with granule cells. Mol. Pharmacol. 25, 24–28.Google Scholar
  197. Wong, D. T., Threlkeld, P. G., Bymaster, F. P. and Squires, R. F. (1984) Saturable binding of [35S]-t-butylbicyclophosphorothionate to the sites linked to the GABA receptor and the interaction with GABAergic agents. Life Sci. 34, 853–860.CrossRefGoogle Scholar
  198. Yamaguchi, I., Matsumura, F. and Kadous, A. A. (1980) Heptachlor epoxide: effects on calcium-mediated transmitter release from brain synaptosomes in rat. Biochem. Pharmacol. 29, 1815–1823.CrossRefGoogle Scholar
  199. Yarowsky, P. J. and Carpenter, D. O. (1978) A comparison of similar ionic responses to γ-aminobutyric acid and acetylcholine. J. Neurophysiol. 41, 531–541.Google Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 1993

Authors and Affiliations

  • N. M. Anthony
    • 1
  • J. B. Harrison
    • 1
  • D. B. Sattelle
    • 1
  1. 1.AFRC Laboratory of Molecular Signalling, Department of ZoologyUniversity of CambridgeCambridgeEngland

Personalised recommendations