Advertisement

The Cloning and Expression in Xenopus laevis Oocytes of an Insect Nicotinic Acetylcholine Receptor α-Subunit

  • John Marshal
  • Eric A. Barnard
  • David B. Sattelle

Abstract

The central nervous system of an insect shares many chemical and some organizational features evident in the more complex nervous systems of vertebrates. In both groups of organisms nerve cells form networks that control behaviour. The functions of an increasing number of uniquely identifiable neurones are established in events such as flight and respiration of insects (Hoyle and Burrows, 1973a,b; Robertson, 1986). In order to understand fully these behaviours it is important to study the molecular components of the system. Of particular interest are the synapses which are control points in the communication between neurones. The chemical synapse plays a major role in neural integration and many different types of neurotransmitter molecules have been recognized such as acetylcholine (ACh), γ-aminobutyric acid (GABA), octopamine and glutamic acid which in turn activate their respective receptors. Although many of these neurotransmitters are also present in the vertebrate CNS, it is becoming increasingly clear that some insect receptors including the nicotinic acetylcholine receptor (nAChR) have different pharmacological properties from those of their vertebrate counterparts (Sattelle, 1980, 1988; Benson, 1988).

Keywords

Nicotinic Acetylcholine Receptor Glycine Receptor Motor Neurone Xenopus Laevis Oocyte nAChR Subunit 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Barnard, E.A., Darlison, M.G., Marshall, J. and Sattelle, D.B. 1989. Structural characterizations of anion and cation channels directly operated by agonists, pp. 159–176 in: “Ion Transport.” Kweeling, D. and Benham, C. eds. Academic Press, London..CrossRefGoogle Scholar
  2. Benson, J.A. 1988a. Transmitter receptors on insect neuronal somata: GABAergic and cholinergic pharmacology, pp. 193–206 in: “Neurotox 1988: Molecular Basis of Drug and Pesticide Action.” G.G. Lunt, ed. Excerpta Medica, Amsterdam.Google Scholar
  3. Benson, J.A., 1988b. Pharmacology of a locust-thoracic ganglion somal nicotinic acetylcholine receptor. pp. 227–240 in: “Nicotinic Receptors in the Nervous System.” Clementi, F., Gotti, C. and Sher, E. eds. Springer Verlag, Berlin.Google Scholar
  4. Blair, L.A.C., Levitan, E.S., Marshall, J., Dionne, V.E. and Barnard, E.A. 1988. Single subunits of the receptor form ion channels with properties of the native receptor. Sciene 242: 577–579.CrossRefGoogle Scholar
  5. Bossy, B., Ballivet, M. and Spierer, P. 1988. Conservation of neuronal nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous system. EMBO. J. 7: 611–618.PubMedGoogle Scholar
  6. Boulter, J., Connolly, J., Deneris, E., Goldman, D., Heinemann, S. and Patrick, J. 1987. Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identified a gene family. Proc. Natl. Acad. Sci. USA. 84: 7763–7767.PubMedCrossRefGoogle Scholar
  7. Breer, H., Kleene, R. and Hinz, G. 1985. Molecular forms and subunit structure of the acetylcholine receptor in the central nervous system of insects. J. Neurosci. 5: 3386–3392.PubMedGoogle Scholar
  8. Buckingham, S.D., Sattelle, D.B. and Hue, B. 1990. Synaptic and extrasynaptic actions of bicuculline on identified insect neurones. J. Exp. Biol. in press.Google Scholar
  9. Carr, C.E. and Fourtner, C.R. 1980. Pharmacological analysis of a monosynaptic reflex in the cockroach Periplaneta americana. J. Exp. Biol. 86: 259–273.Google Scholar
  10. Chiappinelli, V. A., Hue, B., Mony, L. and Sattelle, D.B. 1989. K-Bungarotoxin blocks nicotinic transmission at an identified invertebrate synapse. J. Exp. Biol. 141: 61–71.PubMedGoogle Scholar
  11. David, J.A. and Sattelle, D.B. 1984. Actions of cholinergic pharmacological agents on the cell body membrane of the fast coxal depressor motor neurone of the cockroach Periplaneta americana. J. Exp. Biol. 108: 119–136.Google Scholar
  12. Deneris, E.S., Connolly, J., Boulter, J., Wada, E., Wada, K., Swanson, L.W., Patrick, J. and Heinemann, S. 1988. Primary structure and expression of β2: A novel subunit of neuronal nicotinic acetylcholine receptors. Neuron. 1: 45–54.PubMedCrossRefGoogle Scholar
  13. Freeman, J.A., Schmidt, J.T. and Oswald, R.E. 1980. Effect of α-bungarotoxin in retinotectal synaptic transmission in goldfish and toad. Neurosci. 5: 929–942.CrossRefGoogle Scholar
  14. de la Garza, R., Hoffer, B.J. and Freedman, R. 1988. Heterogeneity of nicotinic actions in the rat cerebellum. pp. 887–891 in: “Nicotinic Acetylcholine Receptors in the Nervous System.” Clementi, F., Gotti, C. and Sher, E., eds. Springer-Verlag, Heidelberg.Google Scholar
  15. Goldman, D., Deneris, E., Luyten, W., Kochlar, A., Patrick, J. and Heinemann, S. 1987. Members of a nicotinic acetylcholine receptor gene family are expressed in different regions of the mammalian central nervous system. Cell 48: 965–973.PubMedCrossRefGoogle Scholar
  16. Grenningloh, G., Rienitz, A., Schmitt, B., Methfessel, C., Zensen, M., Beyreuther, K., Gundelfinger, E.D. and Betz, H.. 1987. The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328: 215–220.PubMedCrossRefGoogle Scholar
  17. Hanke, W. and Breer, H. 1986. Channel properties of a neuronal acetylcholine receptor protein purified from the central nervous system of insect reconstituted in planar lipid bilayers. Nature 321: 171–174.PubMedCrossRefGoogle Scholar
  18. Harrow, I.D., David, J.A. and Sattelle, D.B. 1983. Acetylcholine receptors on identified insect neurones. pp. 12–31 in: “Neuropharmacology of Insects” O’Connor, M. and Whelan, J., eds. Pitman, London.Google Scholar
  19. Harrow, I.D. and Sattelle, D.B. 1982. Acetylcholine receptors on the cell body membrane of giant interneurone 2 in the cockroach Periplaneta americana. J. Exp. Biol. 105: 339–350.Google Scholar
  20. Hermans-Borgmeyer, I., Zopf, D., Ryseck, R.P., Hovemann, B., Betz, H. and Gundelfinger, E.D. 1986. Primary structure of a developmentally regulated nicotinic acetylcholine receptor from Drosophila. EMBO. J. 5: 1503–1508.PubMedGoogle Scholar
  21. Hoyle, G. and Burrows, M. 1973a. Neural mechanisms underlying behavior in the locust Schistocerca gregaria. I. Physiology of identified motor neurons in the metathoracic ganglion. J. Neurobiol. 4: 3–10.PubMedCrossRefGoogle Scholar
  22. Hoyle, G. and Burrows, M. 1973b. Neural mechanisms underlying behavior in the locust Schistocerca gregaria. II. Integrative activity in metathoracic neurons. J. Neurobiol. 4: 43–53.PubMedCrossRefGoogle Scholar
  23. Kao, P.N. and Karlin, A. 1986. Acetylcholine receptor binding site contains a disulphide crosslink between adjacent half-cystinyl residues. J. Biol. Chem. 261: 8085–8090.PubMedGoogle Scholar
  24. Kao, P.N., Dwark, A.J., Kaldany, R.J., Silver, M.L., Widerman, J., Stein, S. and Karlin, A. 1984. Identification of the α-subunit half-cysteine specifically labelled by an affinity reagent for the acetylcholine receptor binding site. J. Biol. Chem. 259: 1162–1168.Google Scholar
  25. Lane, N.J., Swales, L.S., David, J.A. and Sattelle, D.B. 1982. Differential accessibility to two insect neurones does not account for differences in sensitivity to α-bungarotoxin. Tissue Cell 14: 489–500.PubMedCrossRefGoogle Scholar
  26. Lees, G., Beadle, DJ. and Botham, R.P. 1983. Cholinergic receptors on cultured neurones from the CNS of embryonic cockroach. Brain Res. 288: 49–59.PubMedCrossRefGoogle Scholar
  27. Marshall, J., Darlison, M.G., Lunt, G.G. and Barnard, E.A. 1988a. Cloning of a putative nicotinic acetylcholine receptor gene from locust. Biochem. Soc. Trans. 16: 463.PubMedGoogle Scholar
  28. Marshall, J., David, J.A., Darlison, M.G., Barnard, E.A. and Sattelle, D.B. 1988b. Pharmacology, cloning and expression of insect nicotinic acetylcholine receptors. pp 257–281 in: “Nicotinic Acetylcholine Receptors in the Nervous System.” Clementi, F., Gotti, C., and Sher, E., eds. Springer-Verlag, Heidelberg.CrossRefGoogle Scholar
  29. Nef, P., Onegser, C., Alliod, C., Couturiers, S. and Ballivet, M. 1988. Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors. EMBO. J. 7: 595–601.PubMedGoogle Scholar
  30. Numa, S. 1986. Molecular basis for the function of ion channels. pp. 119–143 in: “Molecular Neurobiology.” Kay, J.,ed. Biochemical Society, London.Google Scholar
  31. Pinnock, R.D., Lummis, S.C.R., Chiappinelli, V.A. and Sattelle, D.B. 1988. Actions of potent cholinergic anthelminitics (morantel, pyrantel and levamisole) on an identified insect neurone reveal pharmacological differences between nematode and insect acetylcholine receptors. Neuropharm. 27: 843–848.CrossRefGoogle Scholar
  32. Raftery, M.A., Hunkapiller, M.W., Strader, CD. and Hood, L.E. 1980 Acetylcholine receptor: Complex of homologous subunits. Science 208: 1454–1457.PubMedCrossRefGoogle Scholar
  33. Robertson, R.M. 1986. Neuronal circuits controlling flight in the locust: central generation of rhythm. TINS 9: 278–281.Google Scholar
  34. Sattelle, D.B. 1980. Acetylcholine receptors of insects. Adv. Insect Physiol. 15: 215–315.CrossRefGoogle Scholar
  35. Sattelle, D.B. and David, J.A. 1983. Voltage dependent block by histrionicotoxin of the acetylcholine-induced currents in an insect motorneurone cell body. Neurosci. Lett. 43: 37–41.PubMedCrossRefGoogle Scholar
  36. Sattelle, D.B., Harrow, I.D., Hue, B., Pelhate, M., Gepner, J.I. and Hall, L.M. 1983. α- Bungarotoxin blocks excitatory neurotransmission between cercal sensory neurones and giant interneurone 2 of the cockroach Periplaneta americana. J. Exp. Biol. 107: 473–489.Google Scholar
  37. Sattelle, D.B. 1988. Synaptic and extrasynaptic neuronal nicotinic receptors of insects pp. 563–582, in: “The Molecular Basis of Drug and Pesticide Action.” Lunt, G. C., ed. Elsevier Biomedical Press, Amsterdam.Google Scholar
  38. Schmieden, V., Grenningloh, C., Schofield, P.R. and Betz, H. 1989. Functional expression in Xenopus oocytes of the strychnine binding 48kd subunit of the glycine receptor. EMBO. J. 8: 695–700.PubMedGoogle Scholar
  39. Schofield, P.R., Darlison, M.C., Fujita, N., Burt, D.R., Stephenson, F.A., Rodriguex, H., Rhee, L.M., Ramachandran, J., Reale, V., Glencorse, T.A., Seeburg, P.H. and Barnard, E.A. 1987. Sequence and functional expression of the GABAA receptor shows a ligand-gated receptor superfamily. Nature 328: 221–227.PubMedCrossRefGoogle Scholar
  40. Stephenson, F.A. 1988. Understanding the GABAA receptor: a chemically gated ion channel. Biochem. J. 249: 21–32.PubMedGoogle Scholar
  41. Wafford, K.A. and Sattelle, D.B. 1989. L-glutamate receptors on the cell body membrane of an identified insect motor neurone. J. Exp. Biol. 144: 449–462.Google Scholar
  42. Whiting, P. and Lindstrom, J. 1987. Purification and characterization of a nicotinic acetylcholine receptor from rat brain. Proc. Natl. Acad. Sci. USA 84: 595–600.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • John Marshal
    • 1
  • Eric A. Barnard
    • 2
  • David B. Sattelle
    • 3
  1. 1.Department of PharmacologyYale UniversityUSA
  2. 2.MRC Molecular Neurobiology UnitCambridgeUK
  3. 3.AFRC Unit of Insect Neurophysiology and PharmacologyCambridgeUK

Personalised recommendations