Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-24T01:58:12.428Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular biology and electrophysiology of glutamategated chloride channels of invertebrates

Published online by Cambridge University Press:  06 April 2009

D. F. Cully ,
H. Wilkinson ,
D. K. Vassilatis ,
A. Etter  and
J. P. Arena
D. F. Cully*
Affiliation:
Department of Genetics and Molecular Biology and Department of Cell Biochemistry and Physiology, Merck Research Laboratories, PO 2000, Rahway, New Jersey 07065–0900, USA
*
*Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Summary

In this chapter we summarize the available data on a novel class of ligand-gated anion channels that are gated by the neurotransmitter glutamate. Glutamate is classically thought to be a stimulatory neurotransmitter, however, studies in invertebrates have proven that glutamate also functions as an inhibitory ligand. The bulk of studies conducted in vivo have been on insects and crustaceans, where glutamate was first postulated to act on H-receptors resulting in a hyperpolarizing response to glutamate. Recently, glutamate-gated chloride channels have been cloned from several nematodes and Drosophila. The pharmacology and electrophysiological properties of these channels have been studied by expression in Xenopus oocytes. Studies on the cloned channels demonstrate that the invertebrate glutamate-gated chloride channels are the H-receptors and represent important targets for the antiparasitic avermectins.

Keywords

Glutamateavermectinchloride channelinvertebrates
Type
Research Article
Information
Parasitology , Volume 113 , supplement S1: Molecular biochemistry and physiology of helminth neuromuscular systems , January 1996 , pp. S191 - S200
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arena, J. p. (1994). Expression of Caenorhabditis elegans mRNA in Xenopus oocytes: A model system to study the mechanism of action of avermectins. Parasitology Today 10, 35–7.CrossRefGoogle Scholar
Arena, J. P., Liu, K. K., Cully, D. F., Vassilatis, D. K., Reiss, B. H., Schaeffer, J. M. & Etter, A. (1995a). Characterization of picrotoxin blockade of glutamategated chloride channels reveals structural and functional similarities to GABAA and glycine receptors. Society of Neurosciences Abstracts 21, 1262.Google Scholar
Arena, J. P., Liu, K. K., Paress, P. S. & Cully, D. F. (1991). Avermectin-sensitive chloride currents induced by Caenorhabditis elegans RNA in Xenopus oocytes. Molecular Pharmacology 40, 368–74.Google ScholarPubMed
Arena, J. P., Liu, K. K., Paress, P. S., Frazier, E. G., Cully, D. F., Mrozik, H. & Schaeffer, J. M. (1995a). The mechanism of action of avermectins in Caenorhabditis elegans: correlation between activation of glutamate-sensitive chloride current, membrane binding, and biological activity. Journal of Parasitology 81, 286–94.CrossRefGoogle ScholarPubMed
Arena, J. P., Liu, K. K., Paress, P. S., Schaeffer, J. M. & Cully, D. F. (1992). Expression of a glutamateactivated chloride current in Xenopus oocytes injected with Caenorhabditis elegans RNA: Evidence for modulation with avermectin. Molecular Brain Research 15, 339–48.CrossRefGoogle ScholarPubMed
Avery, L. (1993). Motor-neuron m3 controls pharyngeal muscle-relaxation timing in Caenorhabitis elegans. Journal of Experimental Biology 175, 283–97.CrossRefGoogle Scholar
Bertrand, D. & Changeux, J. P. (1995). Nicotinic receptor: an allosteric protein specialized for intercellular communication. The Neurosciences 7, 75–90.Google Scholar
Betz, H., Langosch, D., Rundstrom, N., Bormann, J., Kuryatov, A., Kuhse, J., Schmieden, V., Matzenbach, B. & KIRSCH, J. (1993). Structure and biology of inhibitory glycine receptors. Annals of the New York Academy of Sciences 707, 109–15.CrossRefGoogle ScholarPubMed
Bolshakov, V. Y., Gapon, S. & Magazanik, L. G. (1991). Different types of glutamate receptors in isolated and identified neurons of the mollusc Planorbarius corneus. Journal of Physiology (London) 439, 15–35.CrossRefGoogle Scholar
Campbell, w. c. (1989). Ivermectin and Abamectin. New York: Springer-Verlag.CrossRefGoogle Scholar
Clark, R. B., Gration, K. A. F. & Usherwood, P. N. R. (1979). Responses to DL-ibotenic acid at locust glutamatergic neuromuscular junctions. British Journal of Pharmacology 66, 267–73.CrossRefGoogle ScholarPubMed
Cleland, T. A. & Selverston, A. I. (1995). Glutamategated inhibitory currents of central pattern generator neurons in the lobster stomatogastric ganglion. Journal of Neuroscience 15, 6631–9.CrossRefGoogle ScholarPubMed
Cull-CANDY, S. G. (1976). Two types of extrajunctional L-glutamate receptors in locust muscle fibres. Journal of Physiology 255, 449–64.CrossRefGoogle ScholarPubMed
Cull-CANDY, S. G. & Usherwood, P. N. R. (1973). Two populations of L-glutamate receptors on locust muscle fibres. Nature, New Biology 246, 62–4.CrossRefGoogle ScholarPubMed
Cully, D. F., Paress, P. S., Liu, K. K., Schaeffer, J. M., et al. (1996). Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. Journal of Biological Chemistry 271, 20187–91.CrossRefGoogle Scholar
Cully, D. F., Vassilatis, D. K., Liu, K. K., Paress, P. S., Van DER PLOEG, L. H. T., Schaeffer, J. M. & Arena, J. P. (1994). Cloning of an avermectin-sensitive glutamategated chloride channel from Caenorhabditis elegans. Nature 371, 707–11.CrossRefGoogle ScholarPubMed
Darlison, M. K. & Albrecht, B. E. (1995). GABAA receptor subtypes: which, where and why? The Neurosciences 7, 115–26.Google Scholar
Delgado, R., Barla, R., Latorre, R. & Labarca, P. (1989). L-Glutamate activates excitatory and inhibitory channels in Drosophila larval muscle. FEBS Letters 243, 337–42.CrossRefGoogle ScholarPubMed
Dubas, F. (1990). Inhibitory effect of L-glutamate on the neuropile arborizations of flight motorneurons in locust. Journal of Experimental Biology 148, 501–8.CrossRefGoogle Scholar
Duce, I. R. & Scott, R. H. (1985a). Actions of dihydroavermectin B12 on insect muscle. British Journal of Pharmacol. 85, 395–401.CrossRefGoogle Scholar
Duce, I. R. & Scott, R. H. (1985b). Interactions of dihydroavermectin Bla, GABA and ibotenic acid on locust (Schistocerca gregaria) muscle. British Journal of Pharmacology 86, 431P.Google Scholar
Dudel, J., Franke, C., Hatt, H. & Usherwood, P. N. R. (1989). Chloride channels gated by extrajunctional glutamate receptors (H-receptors) on locust leg muscle. Brain Research 481, 215–20.CrossRefGoogle ScholarPubMed
Egebjerg, J., Bettler, B., Hermans-BORGMEYER, I. & Heinemann, s. (1991). Cloning of a cDNA for a glutamate receptor subunit subunit activated by kainate but not AMPA. Nature 351, 745–8.CrossRefGoogle Scholar
Etter, A., Cully, D. F., Schaeffer, J. M., Liu, K. K. & Arena, J. p. (1996). An amino acid substitution in the pore region of a glutamate-gated chloride channel enables the coupling of ligand binding to channel gating. Journal of Biological Chemistry 271, 16035–8.CrossRefGoogle ScholarPubMed
Fairman, W. A., Vandenberg, R. J., Arriza, J. L., Kavanaugh, M. p. & Amara, s. G. (1995). An excitatory amino-acid transporter with proerties of a ligandgated chloride channel. Science 375, 599–603.Google Scholar
Ffrench-CONSTANT, R. H., Rocheleau, T. A., Steichen, J. C. & Chalmers, A. E. (1993). A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 363, 449–51.CrossRefGoogle Scholar
Franke, C., Hatt, H. & Dudel, J. (1986). The inhibitory chloride channel activated by glutamate as well as gamino- butyric acid (GABA). Single channel recordings from crayfish muscle. Journal of Comparative Physiology A 159, 591–609.CrossRefGoogle Scholar
Fraser, S. P., Djamgoz, M. B. A., Usherwood, P. N. R., O'BRIEN, J., Darlison, M. G. & Barnard, E. A. (1990). Amino acid receptors from insect muscle: electrophysiological characterization in Xenopus oocytes following expression by injection of mRNA. Molecular Brain Research 8, 331–41.CrossRefGoogle ScholarPubMed
Giles, D. & Usherwood, p. N. R. (1985). The effects of putative amino acid neurotransmitters on somata isolated from neurons of the locust central nervous system. Comparative Biochemistry and Physiology 80C, 231–6.Google Scholar
Grant, G. B. & Dowling, J. E. (1995). A glutamateactivated chloride current in cone-driven ON bipolar cells of the white perch retina. Journal of Neuroscience 15, 3852–62.CrossRefGoogle ScholarPubMed
Horseman, B. G., Seymour, C., Bermudez, I. & Beadle, D. J. (1988). The effect of L-glutamate on cultured insect neurons. Neuroscience Letters 85, 65–70.CrossRefGoogle Scholar
Ikemoto, Y. & Akaike, N. (1988). The glutamate-induced chloride current in Aplysia neurons lacks pharmacological properties seen for excitatory responses. European Journal of Pharmacology 150, 313–8.CrossRefGoogle ScholarPubMed
Johnson, B. R. & Hoooper, s. L. (1992). Overview of the stomatogastric nervous system. In Dynamic Biological Networks: the Stomatogastic Nervous System (ed. Harris-Warrick, R. M., Marder, E., Selverston, A. I. & Moulin, M.), pp. 1–30. Cambridge, MA: MIT Press.Google Scholar
Johnson, B. R., Peck, J. H. & Harris-WARRICK, R. M. (1994). Differential modulation of chemical and electrical components of mixed synapses in the lobster stomatogastric ganglion. Journal of Comparative Physiology 175, 233–49.CrossRefGoogle ScholarPubMed
Keinanen, K., Wisden, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T. A., Sakmann, B. & Seeburg, p. H. (1990). A family of AMPA-selective glutamate receptors. Science 249, 556–60.CrossRefGoogle ScholarPubMed
King, w. M. & Carpenter, D. O. (1987). Distinct GABA and glutamate receptors may share a common channel in Aplysia neurons. Neuroscience Letters 82, 343–8.CrossRefGoogle Scholar
King, W. M. & Carpenter, D. O. (1989). Voltage-clamp characterization of Cl- conductance gated by GABA and L-glutamate in single neurons of Aplysia. Journal of Neurophysiology 61, 892–9.CrossRefGoogle ScholarPubMed
Kuhse, J., Betz, H. & Kirsch, J. (1995). The inhibitory glycine receptor: architecture, synaptic localization and molecular pathology of a postsynaptic ion-channel complex. Current Opinion in Neurobiology 5, 318–23.CrossRefGoogle ScholarPubMed
Laughton, D. L., Wheeler, S. V., Lunt, G. G. & Wolstenholm, A. J. (1995a). The β-subunit of Caenorhabditis elegans avermectin receptor responds to glycine and is encoded by chromosome 1. Journal of Neurochemistry 64, 2354–7.CrossRefGoogle ScholarPubMed
Laughton, D. L., Wolstenholme, A. J. & Lunt, G. (1995b). The β subunit of the C. elegans inhibitory receptor is expressed in the pm4 pharyngeal muscle cells. Journal of Neuroscience 21, 1262.Google Scholar
Lea, T. J. & Usherwood, p. N. R. (1973a). Effect of ibotenic acid on chloride permeability of insect muscle fibres. Comparative General Pharmacology 4, 351–63.CrossRefGoogle ScholarPubMed
Lea, T. J. & Usherwood, p. N. R. (1973b). The site of action of ibotenic acid and the identification of two populations of glutamate receptors on insect musclefibres. Comparative General Pharmacology 4, 333–50.CrossRefGoogle ScholarPubMed
Lingle, C. & Marder, E. (1981). A glutamate-activated chloride conductance on a crustacean muscle. Brain Research 212, 481–8.CrossRefGoogle ScholarPubMed
Marder, E. (1987). Neurotransmitters and neuromodulators. In The Crustacean Stomatogastric System, (ed. Selverston, A. I. & Moulins, M.), pp. 263–306. New York: Springer.CrossRefGoogle Scholar
Marder, E. & Eisen, J. s. (1984). Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. Journal of Neurophysiology 51, 1345–461.CrossRefGoogle ScholarPubMed
Marder, E. & Paupardin-TRITSCH, D. (1978). The pharmacological properties of some crustacean neuronal acetylcholine, GABA, and L-glutamate responses. Journal of Physiology (London) 280, 213–36.CrossRefGoogle ScholarPubMed
Maricq, A. V., Peterson, A. S., Brake, A. J., Myers, R. M. & Julius, D. (1991). Primary structure and functional expression of the 5TH3 receptor, a serotonin-gated ion channel. Science 254, 432–7.CrossRefGoogle ScholarPubMed
Martin, R. J. (1996). An electrophysiological preparation of Ascaris suum pharyngeal muscle reveals a glutamate-gated chloride channel sensitive to the avermectin analogue, milbemycin D. Parasitology 112, 247–52.CrossRefGoogle Scholar
Mat Jais, A. M., Kerkut, G. A. & Walker, R. J. (1984). The ionic mechanims associated with the excitatory response of kainate, L-glutamate, quisqualate, ibotenate, AMPA, and methyltetrahydrofolate on leech Retzius cells. Comparative Biochemistry and Physiology 77C, 115–26.Google Scholar
Moriyoshi, K., Masu, M., Ishii, T., Shigemoto, R., Mizunio, N. & Nakanishi, S. (1991). Molecular cloning and characterization of the rat NMDA receptor. Nature 354, 31–7.CrossRefGoogle ScholarPubMed
Olsen, R. & Tobin, A. (1990). Molecular biology of GABAA receptors. The FASEB Journal 4, 1469–80.CrossRefGoogle ScholarPubMed
Pearlstein, E., Marchand, A. R. & Clarac, F. (1994). Inhibitory effects of L-glutamate on centrol processes of crustacean leg motorneurons. European Journal of Neuroscience 6, 1445–52.CrossRefGoogle Scholar
Pribilla, I., Takagi, T., Langosch, D., Bormann, J. & Betz, H. (1992). The atypical M2 segment of the bsubunit confers picrotoxinin resistance to inhibitory glycine receptors. EMBO Journal 11, 4305–11.CrossRefGoogle Scholar
Sawada, M., Hara, N., Ito, I. & Maeno, T. (1984). Ionic mechanims of hyperopolarizing glutamate effect on two identified neurons in the buccal ganglion of Aplysia. Journal of Neuroscience Research 11, 91–103.CrossRefGoogle Scholar
Schuster, C. M., Ultsch, A., Schloss, P., Cox, J. A., Schmitt, B. & Betz, H. (1991). Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254, 112–4.CrossRefGoogle ScholarPubMed
Scott, R. H. & Duce, I. R. (1985). Effects of 22,23- dihydroavermectin on locust (Schistocerca gregaria) muscles may involve several sites of action. Pesticide Science 16, 599–604.CrossRefGoogle Scholar
Tazaki, K. & Chiba, c. (1994). Glutamate, acetylcholine, and g-aminobutyric acid as transmitters in the pyloric system of the stomatogastric ganglion of a stomatopod, squilla oratorio. Journal of Comparative Physiology A 175, 487–504.CrossRefGoogle Scholar
Ultsch, A., Schuster, C. M., Laube, B., Schloss, P., Schmitt, B. & Betz, H. (1992). Glutamate receptors of Drosophila melanogaster: cloning of a kainate-selective subunit expressed in the central nervous system. Proceedings of the National Academy of Sciences, USA 89, 10484–8.CrossRefGoogle ScholarPubMed
Wadiche, J. I., Amara, S. G. & Kavanaugh, M. P. (1995). Ion fluxes associated with excitatory amino acid transport. Neuron 15, 721–8.CrossRefGoogle ScholarPubMed
Wafford, K. A. & Sattelle, D. B. (1989). L-Glutamate receptors on the cell body membrane of an identified insect motor neurone. Journal of Experimental Biology 144, 449–62.CrossRefGoogle Scholar
Werner, P., Voigrt, M., Keinanen, K., Wisden, W. & Seeburg, P. H. (1991). Cloning of a putative highaffinity kainate receptor expressed predominately in hippocampal CA3 cells. Nature 351, 742–4.CrossRefGoogle Scholar
Wilson, R., Ainscough, R., Anderson, K., Baynes, C., Berks, M., Bonfield, J., Burton, J., Connell, M., Copsey, T., Cooper, J. & Coulson, A. (1994). The C. elegans genome project: contiguous nucleotide sequence of over two megabases from chromosome III. Nature 368, 32–8.CrossRefGoogle Scholar
Zufall, F., Franke, c. & Hatt, H. (1988). Acetylcholine activates a chloride channel as well as glutamate and GABA. Single channel recordings from crayfish stomach and opener muscles. Journal of Comparative Physiology A 163, 609–20.CrossRefGoogle Scholar
Zufall, F., Franke, c. & Hatt, H. (1989). The insecticide avermectin Bla activates a chloride channel in crayfish muscle membrane. Journal of Experimental Biology 142, 191–205.CrossRefGoogle Scholar