Advertisement

Acetylcholine receptor/channel molecules of insects

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

Summary

Acetylcholine-gated ion channels of the nicotinic type are abundant in the nervous system of insects. The channels are permeable to Na+, K+ and probably Ca2+, and unlike most vertebrate neuronal nicotinic acetylcholine receptors the receptor/channel molecule is blocked by α-bungarotoxin (α-Bgt). Such α-Bgt-sensitive receptors are present at synapses and on cell bodies of insect neurones. Single channel recordings have shown the existence of multiple conductances of nAChRs. Studies on several different insect preparations have provided evidence for more than one open state and several closed states of insect nAChRs. Functional insect nAChR channels have now been investigated in situ, following reconstitution of a purified protein in bilayers, and as a result of expressing in Xenopus oocytes messenger RNA encoding receptor subunits.

Molecular cloning of putative nAChR α-subunits and non- α-subunits has been reported from the fruitfly Drosophila melanogaster and the locust Schistocerca gregaria. One of these, αLl, from the locust exhibits many of the pharmacological properties of in situ insect nAChRs when messenger RNA encoding this subunit is expressed in oocytes of Xenopus laevis.

Keywords

Acetylcholine Receptor Xenopus Oocyte Nicotinic Receptor Nicotinic Acetylcholine Receptor Single Channel Conductance 
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. Anderson, C. R., Cull-Candy, S. G., and Miledi, R. (1977) Potential-dependent transition temperature of ionic channels induced by glutamate in locust muscle. Nature 268, 663–665.CrossRefGoogle Scholar
  2. Ballivet, M., Patrick, J., Lee, J., and Heinemann, S. (1982) Molecular cloning of cDNA coding for the gamma subunit of the Torpedo acetylcholine receptor. P.N.A.S. 79, 4466–4470.CrossRefGoogle Scholar
  3. Barnard, E. A., Marshall, J., Darlison, M. G., and Sattelle, D. B. (1989) Structural characteristics of cation and anion channels directly operated by agonists, in: Ion Transport, pp. 159–181. Eds D. J. Keeling and C. D. Benham. Academic Press, London.Google Scholar
  4. Beadle, C. A., Beadle, D. J., Pichon, Y., and Shimahara T. (1985) Patch clamp and noise analysis studies of cholinergic properties of cultured cockroach neurones. J. Physiol. 371, 145.Google Scholar
  5. Beadle D. J., Horseman, G., Pichon, Y., Amar, M., and Shimahara, T. (1989) Acetylcholine-activated ion channels in embryonic cockroach neurones growing in culture. J. exp. Biol. 142, 337–355.Google Scholar
  6. Bossy, B., Ballivet, M., and Spierer, P. (1988) Conservation of neural nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous systems. EM BO J. 7, 611–618.Google Scholar
  7. Boulter, J., Connolly, J., Deneris, E., Goldmann, D., Heinemann, S., and Patrick, J. (1987) Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. P.N.A.S. 84, 7763–7767.CrossRefGoogle Scholar
  8. Brisson, A., and Unwin, N. (1985) Quaternary structure of the acetylcholine receptor. Nature 315, 474–477.CrossRefGoogle Scholar
  9. Breer, H., and Benke, D. (1985) Synthesis of acetylcholine receptors in Xenopus oocytes induced by poly A-mRNA from locust nervous tissue. Naturwissenchaften 72, 213–214.CrossRefGoogle Scholar
  10. Breer, H., and Sattelle, D. B. (1987) Molecular properties and function of insect acetylcholine receptors. J. Insect Physiol. 33, 771–790.CrossRefGoogle Scholar
  11. Cheung, H., Clarke, B. S., and Beadle, D. J. (1991) Action of nitromethylene insecticides on cockroach (Periplaneta americana) cultured neurones. Neurotox. 91, 49–50.Google Scholar
  12. Chialiang, C, and Devonshire, A. L. (1982) Changes in membrane phospholipids, identified by Arrhenius plots of acetylcholinesterase and associated with pyrethroid resistance (kdr) in houseflies (Musca domestica). Pestic. Sci. 13, 156–160.CrossRefGoogle Scholar
  13. Claudio, T., Ballivet, M., Patrick, J., and Heinemann, S. (1983) Nucleotide and deduced amino acid sequences of Torpedo californica acetylcholine receptor γ-subunit. P.N.A.S. 80, 1111–1115.CrossRefGoogle Scholar
  14. Claudio, T. (1990) Molecular genetics of acetylcholine receptor channels, in: Molecular Neurobiology, pp. 63–142. Eds. D. M. Glover and B. D. Hames. IRL series, London.Google Scholar
  15. Colquhoun, D., and Sakmann, B. (1985) Fast events in single-channel currents activated by acetylcholine and its analogues at the frog muscle end-plate. J. Physiol. 369, 501–557.Google Scholar
  16. Couturier, S., Bertrand, D., Marter, J.-M., Hernandez, M.-C, Bertrand, S., Malar, N., Valera, S., Barkar, T., and Ballivet, M. (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-bungarotoxin. Neuron 5, 847–856.CrossRefGoogle Scholar
  17. David, J. A., and Sattelle, D. B. (1984) Action 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
  18. Gardner, P., Ogden, D. C., and Colquhoun, D. (1984) Conductances of single ion channels opened by nicotinic agonists are indistinguishable. Nature 309, 160–162.CrossRefGoogle Scholar
  19. Giraudet, J., Dennis, M., Heidmann, T., Chang, J., and Changeux, J.-P. (1986) Structure of the high-affinity binding site for noncompetitive blockers of the acetylcholine receptor: serine-262 of the subunit is labelled by H3 chlorpromazine. P.N.A.S. 83, 2719–2723.CrossRefGoogle Scholar
  20. Gundelfinger, E. D. (1992) How complex is the nicotinic receptor system of insects? Trends Neurosci. 15, 206–211.CrossRefGoogle Scholar
  21. Hamilton, S., Pratt, D., and Eaton, D. (1985) Arrangement of the subunits of the nicotinic acetylcholine receptor of Torpedo californica as determined by a neurotoxin crosslinking. Biochemistry 24, 2210–2219.CrossRefGoogle Scholar
  22. Hanke, W., Andree, J., Strotmann, J., and Kahle, C. (1990) Functional renaturation of receptor polypeptides eluted from SDS polyacrylamide gels. Eur. Biophys. J. 18, 129–134.CrossRefGoogle Scholar
  23. Hanke, W., and Breer, H. (1986) Channel properties of an insect neuronal acetylcholine receptor protein reconstituted in planar lipid bilayers. Nature 321, 171–174.CrossRefGoogle Scholar
  24. Hanke, W., and Breer, H. (1987) Characterization of the channel properties of a neuronal acetylcholine receptor reconstituted into planar lipid bilayers. J. Gen. Physiol. 90, 855–879.CrossRefGoogle Scholar
  25. Harrison, J. B., Leech, C. A., Katz, J., and Sattelle, D. B. (1990) Embryonic and adult neurones of the housefly (Musca domestica) in culture. Tissue Cell 22, 337–347.CrossRefGoogle Scholar
  26. Hermans-Borgmeyer, I., Zoopf, D., Ryseck, R.-P., Hovemann, B., Betz, H., and Gundelfinger, E. D. (1986) Primary structure of a developmentally regulated nicotinic acetylcholine receptor protein from Drosophila. EM BO J. 5, 1503–1508.Google Scholar
  27. Imoto, K., Methfessel, C., Sakmann, B., Mishina, M., Mori, Y., Konno, T., Fukuda, K., Kurasaki, M., Bujo, H., Fujita, Y., and Numa, S. (1986) Location of a I-subunit region determining ion transport through the acetylcholine receptor channel. Nature 324, 670–674.CrossRefGoogle Scholar
  28. Imoto, K., Busch, C., Sakmann, B., Mishina, M., Konno, T., Nakai, J., Bujo, H., Mori, Y., Fukuda, K., and Numa, S. (1988) Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature 335, 645–648.CrossRefGoogle Scholar
  29. Kao, P. N., Dwork, A. J., Kaldany, R.-R. J., Silver, M. L., Wideman, J., Stein, S., and Karlin, A. (1984) Identification of the subunit half-cysteine specifically labelled by an affinity reagent for acetylcholine receptor binding site. J. Biol. Chem. 259, 11,662–11, 665.Google Scholar
  30. Kao, P., and Karlin, A. (1986) Disulfide crosslink between adjacent half-cystinyl residues as the acetylcholine binding site. Biophys. J. 49, 5a.CrossRefGoogle Scholar
  31. Karlin, A., and Bartels, E. (1966) Effects of blocking sulfhydryl groups and of reducing disulfide bonds on the acetylcholine-activated permeability system of the electroplax. Biochim. Biophys. Acta 126, 525–535.CrossRefGoogle Scholar
  32. Landau, E. M., and Ben-Haim, D. (1974) Acetylcholine noise: Analysis after chemical modification of receptor. Science 185, 944–946.CrossRefGoogle Scholar
  33. Leech, C. A., Bai, D., and Sattelle, D. B. (1992) A sulphydryl reducing agent, dithiothreitol, modifies agonist-nicotinic receptor interaction in an identified insect neurone. J. exp. Biol. 169, 267–270.Google Scholar
  34. Leech, C. A., Jewess, P., Marshall, J., and Sattelle, D. B. (1991) Nitromethylene actions on in situ and expressed insect nicotinic acetylcholine receptors. FEBS Lett. 290, 90–94.CrossRefGoogle Scholar
  35. Leech, C. A., and Sattelle, D. B. (1992) Multiple conductances of neuronal nicotinic acetylcholine receptors. Neuropharmacology 31, 501–507.CrossRefGoogle Scholar
  36. Lindstrom, J., Schopefer, R., and Whiting, P. (1987) Molecular studies of the neural nicotinic acetylcholine receptor family (rev). Mol. Neurobiol. 1, 281–337.CrossRefGoogle Scholar
  37. Marshall, J., Darlison, M. G., Lunt, G. G., and Barnard, E. A. (1988) Cloning of putative nicotinic acetylcholine receptor genes from locust. Biochem. Soc. Trans. 16, 463.Google Scholar
  38. Marshall, J., Buckingham, S. D. Shingai, R., Lunt, G. G., Goosey, M. W., Darlison, M. G., Sattelle, D. B., and Barnard, E. A. (1990) Sequence and functional expression of a single α-subunit of an insect nicotinic acetylcholine receptor. EM BO J. 9 (13) 4391–4398.Google Scholar
  39. Matsuda, H., Saigusa, A., and Irisawa, H. (1987) Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg2+, Nature 325, 156–159.CrossRefGoogle Scholar
  40. Mulle, C., Choquet, D., Korn, H., and Changeux, J.-P. (1992) Calcium influx through nicotinic receptor in rat central neurons: its relevance to cellular regulation. Neuron 8, 135–143.CrossRefGoogle Scholar
  41. Mulle, C., Léna, C., and Changeux, J.-P. (1992) Potentiation of nicotinic receptor response by external calcium in rat central neurons. Neuron 8, 937–945.CrossRefGoogle Scholar
  42. Nef, P., Oneyser, C., Alliod, C., Couturier, S., and Ballivet, M. (1988) Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors. EM BO J. 7, 595–601.Google Scholar
  43. Nelson, N., Anholt, R., Lindstrom, J., and Montal, M. (1980) Reconstruction of purified acetylcholine receptors with functional ion channels in planar lipid bilayers. P.N.A.S. 77, 3057–3061.CrossRefGoogle Scholar
  44. Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Furutani, Y., Hirose, T., Asai, M., Inayama, S., Miyata, T., and Numa, S. (1982) Primary structure of a-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature 299, 793–797.CrossRefGoogle Scholar
  45. Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Kikyotanis, S., Tadaski, H., Asai, M., Takashima, H., Inayama, S., Takashi, M., and Numa, S. (1983) Primary structures of β- and δ-subunit precursors of Torpedo californica acetylcholine receptor deduced from cDNA sequences. Nature 301, 251–255.CrossRefGoogle Scholar
  46. Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Kikyotanis, S., Furutani, Y., Hirose, T., Takashima, H., Inayama, S., Miyata, T., and Numa, S. (1983b) Structural homology of Torpedo californica acetylcholine receptor subunits. Nature 302, 528–532.CrossRefGoogle Scholar
  47. Nomoto, H., Takahashi, N., Nagaki, Y., Endo, S., Arata, Y., and Hayashi, K. (1986) Carbohydrate structures of acetylcholine receptor from Torpedo californica and distribution of oligosaccharides among the subunits. Eur. J. Biochem. 157, 233–242.CrossRefGoogle Scholar
  48. Raftery, M. A., Hunkapiller, M. W., Strader, C. D., and Hood, L. E. (1980) Acetylcholine receptor: complex of homologous subunits. Science 208, 454–457.CrossRefGoogle Scholar
  49. Sattelle, D. B. (1980) Acetylcholine receptors of insects. Adv. Insect Physiol. 15, 215–315.CrossRefGoogle Scholar
  50. Sattelle, D. B. (1986) Insect acetylcholine receptors — biochemical and physiological approaches, in: Neuropharmocology and Pesticide Action, pp. 445–497. Ed. M. G. Ford. Ellis Horwood Ltd.Google Scholar
  51. Sattelle, D. B., Buckingham, S. D., Wafford, K. A., Sherby, S. M., Bakry, N. M., Eldefrawi, A. T., and May, T. E. (1989) Actions of the insecticide 2(nitromethylene) te trahydro-l,3-thiazine on insect and vertebrate nicotinic acetylcholine receptors. Proc. R. Soc. Lond. B 237, 501–514.CrossRefGoogle Scholar
  52. Sattelle, D. B., Sun, Y. A., and Wu, C. F. (1986) Neuronal acetylcholine receptor: patch clamp recording of single channel properties from dissociated insect neurones. IRCS Med. Sci. 14, 65–66.Google Scholar
  53. Sawruk, E., Schloss, P., Betz, H., and Schmitt, B. (1990) Heterogeneity of Drosophila nicotinic acetylcholine receptors: SAD, a novel developmentally regulated α-subunit. EM BO J. 9, 2671–2677.Google Scholar
  54. Schloss, P., Hermans-Borgmeyer, I., Betz, H., and Gundelfinger, E. D. (1988) Neuronal acetylcholine receptors in Drosophila: the ARD protein is a component of a high affinity α-bungarotoxin binding complex. EM BO J. 7, 2889–2894.Google Scholar
  55. Shapiro, R. A., Wakimoto, B. T., Subers, E. M., and Nathanson, N. M. (1989) Characterization and functional expression in mammalian cells of genomic and cDNA clones encloding a Drosophila muscarinic acetylcholine receptor. P.N.A.S. 86, 9039–9043.CrossRefGoogle Scholar
  56. Sombati, S., and Lingle, C. J. (1985) Properties of single acetylcholine (ACh) receptor channels on dissociated CNS neurons of locust and Drosophila. Biophys. J. 47, 258a.Google Scholar
  57. Tareilus, E., Hanke, W., and Breer, H. (1990) Comparative electrophysiological measurements of neuronal acetylcholine receptor channels from insects. J. Comp. Physiol. 167, 521–526.CrossRefGoogle Scholar
  58. Unwin, N. (1989) The structure of ion channels in membranes of excitable cells. Neuron 3, 665–676.CrossRefGoogle Scholar
  59. Unwin, N., Toyoshima, C., and Kubalke, E. (1988) Arrangement of the acetylcholine receptor subunits in the resting and desensitized stages, determined by cryoelectron microscopy of crystallized Torpedo postsynaptic membranes. J. Cell Biol. 107, 1123–1138.CrossRefGoogle Scholar
  60. Vernino, S., Amador, M., Luetje, C. W., Patrick, J., and Dani, J. A. (1992) Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8, 127–134.CrossRefGoogle Scholar
  61. Wada, E., Ballivet, M., Boulter, J., Connolly, J., Wada, E., Deneris, E. S., Swanson, L. W., Heinemann, S., and Patrick, J. (1988) Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor. Science 240, 330–334.CrossRefGoogle Scholar
  62. Wadsworth, S. C., Rosenthal, L. S., Kammermeyer, K. L., Potter, M. B., and Nelson, D. J. (1988) Expression of a Drosophila melanogaster acetylcholine receptor-related gene in the central nervous system. Mol. Cell Biol. 8, 778–785.Google Scholar
  63. Whiting, P., and Lindstrom, J. (1987) Purification and characterization of a nicotinic acetylcholine receptor from rat brain. P.N.A.S. 84, 595–599.CrossRefGoogle Scholar
  64. Wise, D. S., Wall, J., and Karlin, A. (1981) Relative locations of the beta and delta chains of the acetylcholine receptor determined by electron microscopy of isolated receptor trimer. J. Biol. Chem. 256, 12,624–12, 627.Google Scholar
  65. Witzemann, V., Barg, B., Nishikawa, Y., Sakmann, B., and Numa, S. (1987) Differential regulation of muscle acetylcholine receptor γ- and ε-subunit mRNA. FEBS Lett. 223, 103–112.CrossRefGoogle Scholar
  66. Wu, C. F., Suzuki, N., and Poo, M. M. (1983) Dissociated neurons from normal and mutant Drosophila larval central nervous system in cell culture. J. Neurosci. 3, 1888–1899.Google Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 1993

Authors and Affiliations

  1. 1.AFRC Laboratory of Molecular Signalling, Department of ZoologyUniversity of CambridgeCambridgeEngland

Personalised recommendations