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Channel blocking drugs as tools to study glutamate receptors in insect muscles and molluscan neurons

  • Articles from the ICINN 97 Conference
  • Neurotoxins and Channel Blockers
  • Published:
Invertebrate Neuroscience

Abstract

The action of three dicationic drugs, derivatives of adamantane (IEM-1460 and IEM-1754) and phencyclidine (IEM-1925), on glutamate receptors (GluRs) at the insect neuromuscular junction (Calliphora vicina larva) and on neurons of the freshwater gastropodian molluscPlanorbarius corneus has been studied using the voltage clamp technique. In the presence of concanavalin A complex glutamate-induced currents recorded from molluscan neurons reflected mainly the opening of cationic channels as a result of decreased desensitisation and inhibition of a chloride component. Under these conditions all drugs studied inhibited the stationary component of glutamate-gated cationic currents in a dose-dependent manner (IC50s were 0.1 μM, 1.0 μM and 19.2 μM for the action of IEM-1925, IEM-1460 and IEM-1754 respectively). The same rank order of potency: IEM-1925 > IEM-1460 > IEM-1754 was observed in both the insect and mollusc. The results of these experiments are compared with those obtained earlier on vertebrate GluRs. Open-channel blocking drugs may help to identify and classify GluRs of invertebrates, and could be used as tools to elucidate the involvement of GluRs in the transmission at certain synapses.

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References

  • Antonov, S. M., Dudel, J., Franke, C. and Hatt, H. (1989) Argiopine blocks glutamate-activated single-channel currents on crayfish muscle by two mechanisms.J. Physiol. (Lond.),419, 569–587.

    CAS  Google Scholar 

  • Antonov, S. M., Johnson, J. W., Lukomskaya, N. Y., Potapjeva, N. N., Gmiro, V. E. and Magazanik, L. G. (1995) Novel adamantane derivatives act as blockers of open ligand-gated channels and as anticonvulsants.Mol. Pharmacol.,47, 558–567.

    PubMed  CAS  Google Scholar 

  • Arvanov, V. L., Tsai, M. C., Walker, R. J. and Ayrapetyan, S. N. (1993) Interaction of concanavalin-A and wheat germ agglutinin withHelix acetylcholine receptors.Brain Res.,615, 252–258.

    Article  PubMed  CAS  Google Scholar 

  • Arvanov, V. L., Chou, H. C., Chen, Y. H., Chen, R. C., Chang, Y. C. and Tsai, M. C. (1995) Effects of concanavalin A on desensitisation kinetics of GABA responses inAchatina fulica neurons.Cell Biol. Toxicol.,11, 113–118.

    Article  PubMed  CAS  Google Scholar 

  • Bahls, F. H., Emery, D. G. and Haydon, P. G. (1995) Glutamatemediated synaptic transmission between neuron B4 and salivary cells ofHelisoma trivolvis.Invertebrate Neurosci.,1, 123–131.

    Article  CAS  Google Scholar 

  • Blaschke, M., Keller, B. U., Rivosecchi, R., Hollmann, M., Heinemann, S. and Konnerth, A. (1993) A single amino acid determines the subunit-specific spider toxin block of α-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor channels.Proc. Natl. Acad. Sci. USA,90, 6528–6532.

    Article  PubMed  CAS  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 molluscPlanorbarius corneus.J. Physiol. (Lond.),439, 15–35.

    CAS  Google Scholar 

  • Bolshakov, V. Y., Gapon, S. A. and Magazanik, L. G. (1992) Transduction mechanism for glutamate-induced potassium current in neurones of the molluscPlanorbarius corneus.J. Physiol. (Lond.),455, 33–50.

    CAS  Google Scholar 

  • Bolshakov, V. Y., Gapon, S. A., Katchman, A. N. and Magazanik, L. G. (1993) Activation of a common potassium channel in molluscan neurones by glutamate, dopamine and muscarinic agonist.J. Physiol. (Lond.) 468, 11–33.

    CAS  Google Scholar 

  • Brackley, P. T. H., Bell, D. R., Choi, S. K., Nakanishi, K. and Usherwood, P. N. R. (1993) Selective antagonism of native and cloned kainate and NMDA receptors by polymine-containing toxins.J. Pharmacol. Exp. Ther.,266, 1573–1580.

    PubMed  CAS  Google Scholar 

  • Brundell, P., Goodnow, R., Jr., Kerry, C. J., Nakanishi, K., Sudan, H. L. and Usherwood, P. N. (1991) Quisqualate-sensitive glutamate receptors of the locustSchistocerca gregaria are antagonised by intracellularly applied philanthotoxin and spermine.Neurosci. Lett.,131, 196–200.

    Article  PubMed  CAS  Google Scholar 

  • Burnashev, N., Monyer, H., Seeburg, P. H. and Sakmann, B. (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit.Neuron,8, 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Chang, H., Ciani, S. and Kidokoro, Y. (1994) Ion permeation properties of the glutamate receptor channel in cultured embryonicDrosophila myotubes.J. Physiol. (Lond.),476.1, 1–16.

    Google Scholar 

  • Clark, R. B., Donaldson, P. L., Gration, K. A. F., Lambert, J. J., Piek, T., Ramsey, R., Spanjer, W. and Usherwood, P. N. R. (1982) Block of locust muscle glutamate receptor by delta-philanthotoxin occurs after receptor activation.Brain Res.,241, 105–114.

    Article  PubMed  CAS  Google Scholar 

  • Cleland, T. A. (1996) Inhibitory glutamate receptor channels.Molec. Neurobiol.,13, 97–136.

    CAS  Google Scholar 

  • Cull-Candy, S. G. (1976) Two types of extrajunctional L-glutamate receptors in locust muscle fibres.J. Physiol. (Lond.),255, 449–464.

    CAS  Google Scholar 

  • Darlison, M. G. (1992) Invertebrate GABA and glutamate receptors: molecular biology reveals predictable structures but some unusual pharmacologies.Trends Neurosci.,15, 469–474.

    Article  PubMed  CAS  Google Scholar 

  • Dierkes, P. W., Hochstrate, P. and Schlue, W. R. (1996) Distribution and functional properties of glutamate receptors in the leech central nervous system.J. Neurophysiol.,75, 3212–2322.

    Google Scholar 

  • Gapon, S. A. (1983) The effect of putative transmitters on identified neurones of the gastropod molluscPlanorbarius comeus.Z. Evol. Biokh. I. Fiziol.,19, 38–45 (in Russian).

    CAS  Google Scholar 

  • Gapon S. A. and Samoilova M. V. (1982) The dercease of membrane conductance of isolated neurones under the action of putative transmitters in the molluscPlanorbarius corneus.Z. Evol. Biokh. I. Fiziol.,18, 535–538 (in Russian).

    CAS  Google Scholar 

  • Ger, B. A., Katchman, A. N. and Zeimal, E. V. (1979) Biphasic acetylcholine responses of molluscan neurones: their dependence on acetylcholine concentration.Brain Res.,167, 426–430.

    Article  PubMed  CAS  Google Scholar 

  • Herlitze, S., Raditsch, M., Ruppersberg, J. P., Jahn, W., Monyer, H., Schoepfer, R. and Witzemann, V. (1993) Argiotoxin detects molecular differences in AMPA receptor channels.Neuron,10, 1131–1140.

    Article  PubMed  CAS  Google Scholar 

  • Hollmann, M. and Heinemann, S. F. (1994) Cloned glutamate receptors.Annu. Rev. Neurosci.,17, 31–108.

    Article  PubMed  CAS  Google Scholar 

  • Hume, R. I., Dingledine, R. and Heinemann, S. F. (1991). Identification of a site in glutamate receptor subunits that controls calcium permeability.Science,253, 1028–1031.

    PubMed  CAS  Google Scholar 

  • Iino, M., Koike, M., Isa, T. and Ozawa, S. (1996) Voltage-dependent blockade of Ca2+-permeable AMPA receptors by Joro spider toxin in cultured rat hippocampal neurones.J. Physiol. (Lond.),424, 151–165.

    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. Pharmacol.,150, 313–318.

    Article  PubMed  CAS  Google Scholar 

  • Jan, L. Y. and Jan Y. N. (1976) L-Glutamate as an excitatory transmitter at theDrosophila larval neuromuscular junction.J. Physiol. (Lond.),262, 215–236.

    CAS  Google Scholar 

  • Katz, P. S. and Levitan, I. B. (1993) Quisqualate and ACPD are agonists for a glutamate-activated current in identifiedAplysia neurons.J. Neurophysiol.,69, 143–150.

    PubMed  CAS  Google Scholar 

  • Kehoe, J. S. (1978) Transformation by concanavalin A of the response of molluscan neurones to L-glutamate.Nature,274, 866–869.

    Article  PubMed  CAS  Google Scholar 

  • Kerry, C. J., Ramsey, R. L., Sansom, M. S. P. and Usherwood, P. N. R. (1988) Single channel studies of non-competitive antagonism of a quisqualate-sensitive glutamate receptor by argiotoxin-636-a fraction isolated from orb-web spider venom.Brain Res.,459, 312–327.

    Article  PubMed  CAS  Google Scholar 

  • Lea, T. J. and Usherwood, P. N. R. (1973) The site of action of ibotenic acid and the identification of two populations of glutamate receptors on insect muscle fibres.Comp. Gen. Pharmacol.,4, 333–350.

    Article  PubMed  CAS  Google Scholar 

  • Lingle, C. and Marder, E. (1981) A glutamate-activated chloride conductance on a crustacean muscle.Brain Res.,212, 481–488.

    Article  PubMed  CAS  Google Scholar 

  • Magazanik, L. G. (1996) Spider neurotoxins as tools for the investigation of glutamate receptors.Toxin Rev.,15, 59–76.

    CAS  Google Scholar 

  • Magazanik, L. G., Antonov, S. M., Fedorova, I. M., Volkova, T. M. and Grishin, E. V. (1986) Argiopin-a naturally occurring blocker of glutamate-sensitive synaptic channels.Biol. Membrany,3, 1204–1219 (in Russian).

    Google Scholar 

  • Magazanik, L. G., Antonov, S. M. and Gmiro, V. E. (1984) Kinetics and pharmacological blockade of glutamate-activated postsynaptic ion channels.Biol. Membrany 1, 130–140 (in Russian).

    CAS  Google Scholar 

  • Magazanik, L. G., Antonov, S. M., Lukomskaya, N. Y., Potapjeva, N. N., Gmiro, V. E. and Johnson, J. W. (1994) Admantane derivative induced block of acetylcholine, glutamate and NMDA activated open channels.Fiziol. Z.,80, 99–112 (in Russian).

    CAS  Google Scholar 

  • Magazanik, L. G., Buldakova, S. A., Samoilova, M. V., Gmiro, V. E., Mellor, I. and Usherwood, P. N. R. (1997a) Block of open channels of recombinant AMPA receptors and native AMPA/kainate receptors by admantane derivatives.J. Physiol. (Lond.),505.3, 655–663.

    Article  Google Scholar 

  • Magazanik, L. G., Buldakova, S. A., Samoilova, M. V., Mellor, I. and Usherwood, P. N. (1997b) Non-competitive antagonism of cloned and native AMPA/kainate receptors by adamantane derivatives.J. Physiol. (Lond.),501, 17P.

    Google Scholar 

  • Mathers, D. A. and Usherwood, P. N. R. (1976) Concanavalin A blocks desensitisation of glutamate receptors on insect muscle fibres.Nature,259, 409–411.

    Article  PubMed  CAS  Google Scholar 

  • Samoilova, M. V., Frolova, E. V. and Magazanik, L. G. (1997) Glutamate receptors controlling cationic channels in the neurons of gastropod molluscPlanorbarius corneus.Z. Evol. Biokh. I. Fiziol.,33, 331–346 (in Russian).

    Google Scholar 

  • Sudan, H. L., Kerry, C. J., Mellor, I. R., Choi, S.-K., Huang, D., Nakanishi, K. and Usherwood, P. N. R. (1995) The action of philanthotoxin-343 and photolabile analogues on locust (Schistocerca gregaria) muscle.Invertebrate Neurosci.,1, 139–172.

    Google Scholar 

  • Stühmer, T., Amar, M., Harvey, R. J., Van Minnen, J. and Darlison, M. G. (1996) Structure and pharmacological properties of a molluscan glutamate-gated cation channel and its likely role in feeding behaviour.J. Neurosci.,16, 2869–2880.

    PubMed  Google Scholar 

  • Tsubokawa, H., Oguro, K., Masuzawa, T., Nakaima, T. and Kawai, N. (1995) Effects of a spider toxin and its analogue on glutamate-activated currents in the hippocampal CAI neuron after ischemia.J. Neurophysiol.,74, 218–225.

    PubMed  CAS  Google Scholar 

  • Usherwood, P. N. R. and Blagbrough, I. S. (1991) Spider toxins affecting glutamate receptors: polyamines in therapeutic neurochemistry.Pharmacol. Therap.,52, 245–268.

    Article  CAS  Google Scholar 

  • Washburn, M. S., Numberger, M., Zhang, S. and Dingledine, R. (1997) Differential dependence on GluR2 expression of three characteristic features of AMPA receptors.J. Neurosci.,17, 9393–9406.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    M. V. Samoilova, E. V. Frolova, N. N. Potapjeva, I. M. Fedorova & L. G. Magazanik

  2. Institute of Experimental Medicine, Russian Medical Academy of Sciences, St. Petersburg, Russia

    V. E. Gmiro

Authors
  1. M. V. Samoilova
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  2. E. V. Frolova
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  3. N. N. Potapjeva
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  4. I. M. Fedorova
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  5. V. E. Gmiro
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  6. L. G. Magazanik
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Correspondence to L. G. Magazanik.

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Samoilova, M.V., Frolova, E.V., Potapjeva, N.N. et al. Channel blocking drugs as tools to study glutamate receptors in insect muscles and molluscan neurons. Invertebrate Neuroscience 3, 117–126 (1997). https://doi.org/10.1007/BF02480366

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  • DOI: https://doi.org/10.1007/BF02480366

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