Skip to main content
SpringerLink
Log in

Molluscan ligand-gated ion-channel receptors

  • Chapter
Comparative Molecular Neurobiology

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

Summary

In this chapter we introduce the reader to the structures of the different types of ligand-gated ion-channel receptor, and the numerous receptor subtypes that have recently been revealed to exist, in both invertebrate and vertebrate species, by the application of molecular biological methods. We then review some of the data in support of the existence, in molluscs, of such receptor/channel complexes for γ-aminobutyric acid, glutamate and acetylcholine. Finally, recent results from our laboratory on the cloning and expression of complementary DNAs, from the pond-snail Lymnaea stagnalis, that encode GABAA and glutamate receptor subunits will be described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Azanza, M. J. and Walker, R. J. (1975) GABA-receptor interactions; models in Helix aspersa neurons. Comp. Biochem. Physiol. 50C, 155–161.

    Google Scholar 

  • Barnard, E. A., Darlison, M. G. and Seeburg, P. (1987) Molecular biology of the GABAA receptor: the receptor/channel superfamily. Trends Neurosci. 10, 502–509.

    Article  Google Scholar 

  • Bateson, A. N., Lasham, A. and Darlison, M. G. (1991a) γ-Aminobutyric acidA receptor heterogeneity is increased by alternative splicing of a novel β-subunit gene transcript. J. Neurochem. 56, 1437–1440.

    Article  Google Scholar 

  • Bateson, A. N., Harvey, R. J., Wisden, W., Glencorse, T. A., Hicks, A. A., Hunt, S. P., Barnard, E. A. and Darlison, M. G. (1991b) The chicken GABAA receptor αl subunit: cDNA sequence and localization of the corresponding mRNA. Molec. Brain Res. 9, 333–339.

    Article  Google Scholar 

  • Bettler, B., Boulter, J., Hermans-Borgmeyer, I., O’Shea-Greenfield, A., Deneris, E. S., Moll, C., Borgmeyer, U., Hollmann, M. and Heinemann, S. (1990) Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583–595.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bolshakov, V. Y., Gapon, S. A. and Magazanik, L. G. (1991) Different types of glutamate receptors in isolated and identified neurones of the mollusc Planorbarius corneus. J. Physiol. 439, 15–35.

    Google Scholar 

  • Boulter, J., Hollmann, M., O’Shea-Greenfield, A., Hartley, M., Deneris, E., Maron, C. and Heinemann, S. (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249, 1033–1037.

    Article  Google Scholar 

  • Cooper, E., Couturier, S. and Ballivet, M. (1991) Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature 350, 235–238.

    Article  Google Scholar 

  • Couturier, S., Bertrand, D., Matter, J.-M., Hernandez, M.-C., Bertrand, S., Millar, N., Valera, S., Barkas, T. and Ballivet, M. (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5, 847–856.

    Article  Google Scholar 

  • Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I. and Heinemann, S. (1991) Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351, 745–748.

    Article  Google Scholar 

  • ffrench-Constant, R. H., Mortlock, D. P., Shaffer, C. D., MacIntyre, 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.

    Article  Google Scholar 

  • Frohman, M. A. and Martin, G. R. (1989) Rapid amplification of cDNA ends using nested primers. Technique 1, 165–170.

    Google Scholar 

  • Frohman, M. A., Dush, M. K. and Martin, G. R. (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl Acad. Sci. USA 85, 8998–9002.

    Article  Google Scholar 

  • Ger, B. A. and Zeimal, E. V. (1977) Pharmacological study of two kinds of cholinoreceptors on the membrane of identified completely isolated neurones of Planorbarius corneus. Brain Res. 121, 131–149.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Grenningloh, G., Pribilla, I., Prior, P., Multhaup, G., Beyreuther, K., Taleb, O. and Betz, H. (1990a) Cloning and expression of the 58 kd β subunit of the inhibitory glycine receptor. Neuron 4, 963–970.

    Article  Google Scholar 

  • Grenningloh, G., Schmieden, V., Schofield, P. R., Seeburg, P. H., Siddique, T., Mohandas, T. K., Becker, C.-M. and Betz, H. (1990b) Alpha subunit variants of the human glycine receptor: primary structures, functional expression and chromosomal localization of the corresponding genes. EM BO J. 9, 771–776.

    Google Scholar 

  • 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 chimeric receptor with a vertebrate α subunit. EM BO J. 10, 3239–3245.

    Google Scholar 

  • 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 protein from Drosophila. EM BO J. 5, 1503–1508.

    Google Scholar 

  • Hollmann, M., O’Shea-Greenfield, A., Rogers, S. W. and Heinemann, S. (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342, 643–648.

    Article  Google Scholar 

  • Hutton, M. L., Harvey, R. J., Barnard, E. A. and Darlison, M. G. (1991) Cloning of a cDNA that encodes an invertebrate glutamate receptor subunit. FEBS Lett. 292, 111–114.

    Article  Google Scholar 

  • Ikemoto, Y. and Akaike, N. (1988) The glutamate-induced chloride current in Aplysia neurones lacks pharmacological properties seen for excitatory responses to glutamate. Eur. J. Pharmac. 150, 313–318.

    Article  Google Scholar 

  • Jonas, P., Baumann, A., Merz, B. and Gundelfinger, E. D. (1990) Structure and developmental expression of the Dα2 gene encoding a novel nicotinic acetylcholine receptor protein of Drosophila melanogaster. FEBS Lett. 269, 264–268.

    Article  Google Scholar 

  • Katchman, A. N. and Zeimal, E. V. (1982) Ionic mechanisms of the rapid (nicotinic) phase of acetylcholine response in identified Planobarius corneus neurones. Brain Res. 241, 95–103.

    Google Scholar 

  • Kehoe, J. (1972a) Ionic mechanisms of a two-component cholinergic inhibition in Aplysia neurones. J. Physiol. 225, 85–114.

    Google Scholar 

  • Kehoe, J. (1972b) Three acetylcholine receptors in Aplysia neurones. J. Physiol. 225, 115–146.

    Google Scholar 

  • Kehoe, J., Sealock, R. and Bon, C. (1976) Effects of α-toxins from Bungarus multicinctus and Bungarus caeruleus on cholinergic responses in Aplysia neurones. Brain Res. 107, 527–540.

    Article  Google Scholar 

  • Keinänen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T. A., Sakmann, B. and Seeburg, P. H. (1990) A family of AMPA-selective glutamate receptors. Science 249, 556–560.

    Article  Google Scholar 

  • King, W. M. and Carpenter, D. O. (1987) Distinct GABA and glutamate receptors may share a common channel in Aplysia neurons. Neurosci. Lett. 82, 343–348.

    Article  Google Scholar 

  • King, W. M. and Carpenter, D. O. (1989) Voltage-clamp characterization of CI conductance gated by GABA and L-glutamate in single neurons of Aplysia. J. Neurophysiol. 61, 892–899.

    Google Scholar 

  • Kuhse, J., Schmieden, V. and Betz, H. (1990) Identification and functional expression of a novel ligand binding subunit of the inhibitory glycine receptor. J. Biol. Chem. 265, 22317–22320.

    Google Scholar 

  • Kuhse, J., Kuryatov, A., Maulet, Y., Malosio, M. L., Schmieden, V. and Betz, H. (1991) Alternative splicing generates two isoforms of the α2 subunit of the inhibitory glycine receptor. FEBS Lett. 283, 73–77.

    Article  Google Scholar 

  • Lüddens, H., Pritchett, D. B., Köhler, M., Killisch, I., Keinänen, K., Monyer, H., Sprengel, R. and Seeburg, P. H. (1990) Cerebellar GABAA receptor selective for a behavioural alcohol antagonist. Nature 346, 648–651.

    Article  Google Scholar 

  • Malosio, M.-L., Marqueze-Pouey, B., Kuhse, J. and Betz, H. (1991a) Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EM BO J. 10, 2401–2409.

    Google Scholar 

  • Malosio, M.-L., Grenningloh, G., Kuhse, J., Schmieden, V., Schmitt, B., Prior, P. and Betz, H. (1991b) Alternative splicing generates two variants of the α1 subunit of the inhibitory glycine receptor. J. Biol. Chem. 266, 2048–2053.

    Google Scholar 

  • Maricq, A. V., Peterson, A. S., Brake, A. J., Myers, R. M. and Julius, D. (1991) Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel. Science 254, 432–437.

    Article  Google Scholar 

  • 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, 4391–4398.

    Google Scholar 

  • Mishina, M., Takai, T., Imoto, K., Noda, M., Takahashi, T., Numa, S., Methfessel, C. and Sakmann, B. (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321, 406–411.

    Article  Google Scholar 

  • Moriyoshi, K., Masu, M., Ishii, T., Shigemoto, R., Mizuno, N. and Nakanishi, S. (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354, 31–37.

    Article  Google Scholar 

  • Morris, B. J., Hicks, A. A., Wisden, W., Darlison, M. G., Hunt, S. P. and Barnard, E. A. (1990) Distinct regional expression of nicotinic acetylcholine receptor genes in chick brain. Molec. Brain Res. 7, 305–315.

    Article  Google Scholar 

  • 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 α-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature 299, 793–797.

    Article  Google Scholar 

  • Olsen, R. W. and Tobin, A. J. (1990) Molecular biology of GABAA receptors. FASEB J. 4, 1469–1480.

    Google Scholar 

  • Oyama, Y., Ikemoto, Y., Kits, K. S. and Akaike, N. (1990) GABA affects the glutamate receptor-chloride channel complex in mechanically isolated and internally perfused Aplysia neurons. Eur. J. Pharmac. 185, 43–52.

    Article  Google Scholar 

  • Piggott, S. M., Kerkut, G. A. and Walker, R. J. (1977) The actions of Picrotoxin, strychnine, bicuculline and other convulsants and antagonists on the responses to acetylcholine glutamic acid and gamma-aminobutyric acid on Helix neurones. Comp. Biochem. Physiol. 57C, 107–116.

    Google Scholar 

  • Popot, J.-L. and Changeux, J.-P. (1984) Nicotinic receptor of acetylcholine: structure of an oligomeric integral membrane protein. Physiol. Rev. 64, 1162–1239.

    Google Scholar 

  • Pritchett, D. B., Lüddens, H. and Seeburg, P. H. (1989) Type I and type II GABAA-benzodiazepine receptors produced in transfected cells. Science 245, 1389–1392.

    Article  Google Scholar 

  • Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B. and Erlich, H. A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487–491.

    Article  Google Scholar 

  • Sawruk, E., Schloss, P., Betz, H. and Schmitt, B. (1990a) Heterogeneity of Drosophila nicotinic acetylcholine receptors: SAD, a novel developmentally regulated α-subunit. EM BO J. 9, 2671–2677.

    Google Scholar 

  • Sawruk, E., Udri, C., Betz, H. and Schmitt, B. (1990b) SBD, a novel structural subunit of the Drosophila nicotinic acetylcholine receptor, shares its genomic localization with two α-subunits. FEBS Lett. 273, 177–181.

    Article  Google Scholar 

  • Schoepfer, R., Conroy, W. G., Whiting, P., Gore, M. and Lindstrom, J. (1990) Brain α-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5, 35–48.

    Article  Google Scholar 

  • 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 functional expression of the GABAA receptor shows a ligand-gated receptor super-family. Nature 328, 221–227.

    Article  Google Scholar 

  • Schuster, C. M., Ultsch, A., Schloss, P., Cox, J. A., Schmitt, B. and Betz, H. (1991) Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254, 112–114.

    Article  Google Scholar 

  • Sigel, E., Baur, R., Malherbe, P. and Möhler, H. (1989) The rat β1-subunit of the GABAA receptor forms a picrotoxin-sensitive anion channel open in the absence of GABA. FEBS Lett. 257, 377–379.

    Article  Google Scholar 

  • Sigel, E., Baur, R., Trübe, G., Möhler, H. and Malherbe, P. (1990) The effect of subunit composition of rat brain GABAA receptors on channel function. Neuron 5, 703–711.

    Article  Google Scholar 

  • Sommer, B., Keinänen, K., Verdoorn, T. A., Wisden, W., Burnashev, N., Herb, A., Köhler, M., Takagi, T., Sakmann, B. and Seeburg, P. H. (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580–1585.

    Article  Google Scholar 

  • Vehovszky, A., Bokisch, A. J., Krogsgaard-Larsen, P. and Walker, R. J. (1989) Pharmacological profile of gamma-aminobutyric acid (GABA) receptors of identified central neurones from Helix aspersa. Comp. Biochem. Physiol. 92C, 391–399.

    Article  Google Scholar 

  • Verdoorn, T. A., Burnashev, N., Monyer, H., Seeburg, P. H. and Sakmann, B. (1991) Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252, 1715–1718.

    Article  Google Scholar 

  • Werner, P., Voigt, M., Keinanen, K., Wisden, W. and Seeburg, P. H. (1991) Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 351, 742–744.

    Article  Google Scholar 

  • Whiting, P., McKernan, R. M. and Iversen, L. L. (1990) Another mechanism for creating diversity in γ-aminobutyrate 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. Scl. USA 87, 9966–9970.

    Article  Google Scholar 

  • Wilson-Shaw, D., Robinson, M., Gambarana, C., Siegel, R. E. and Sikela, J. M. (1991) A novel γ subunit of the GABAA receptor identified using the polymerase chain reaction. FEBS Lett. 284, 211–215.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Yarowsky, P. J. and Carpenter, D. O. (1976) Aspartate: distinct receptors on Aplysia neurons. Science 192, 807–809.

    Article  Google Scholar 

  • Yarowsky, P. J. and Carpenter, D. O. (1978a) Receptors for gamma-aminobutyric acid (GABA) on Aplysia neurons. Brain Res. 144, 75–94.

    Article  Google Scholar 

  • Yarowsky, P. J. and Carpenter, D. O. (1978b) A comparison of similar ionic responses to γ-aminobutyric acid and acetylcholine. J. Neurophysiol. 41, 531–541.

    Google Scholar 

  • Yongsiri, A., Funase, K., Takeuchi, H., Shimamoto, K. and Ohfune, Y. (1988) Classification of GABA receptors in snail neurones. Eur. J. Pharmac. 155, 239–245.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Zellbiochemie und klinische Neurobiologie, Universitäts-Krankenhaus Eppendorf, Universität Hamburg, Martinistrasse 52, 2000, Hamburg 20, Germany

    Mark G. Darlison & Robert J. Harvey

  2. MRC Molecular Neurobiology Unit, MRC Centre, Hills Road, Cambridge, CB2 2QH, England

    Michael L. Hutton

Authors
  1. Mark G. Darlison
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael L. Hutton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert J. Harvey
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Equipe de Neurobiologie, C.N.R.S.-Université de Rennes I, Bât. 13-Complexe Univ. de Beaulieu, F-35042, Rennes Cedex, France

    Yves Pichon

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Birkhäuser Verlag Basel/Switzerland

About this chapter

Cite this chapter

Darlison, M.G., Hutton, M.L., Harvey, R.J. (1993). Molluscan ligand-gated ion-channel receptors. In: Pichon, Y. (eds) Comparative Molecular Neurobiology. EXS, vol 63. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-7265-2_3

Download citation

  • DOI: https://doi.org/10.1007/978-3-0348-7265-2_3

  • Publisher Name: Birkhäuser Basel

  • Print ISBN: 978-3-0348-7267-6

  • Online ISBN: 978-3-0348-7265-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation