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Modulatory Role of Adenosine Receptors in Insect Motor Nerve Terminals

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Abstract

The effects of adenosine and ATP were studied on blowfly larvae Calliphora vicina neuromuscular preparation. Adenosine diminished (IC50 = 40 ± 3 μM) the amplitude of nerve-evoked postsynaptic currents (EPSCs) and slightly decreased the frequency of spontaneous currents without affecting their amplitude. EPSCs were slightly reduced by ATP, and this effect was prevented by concanavalin A. Presynaptic inhibition by adenosine was temperature-dependent and insensitive to pertussis toxin. A1 agonists of vertebrate adenosine receptor CPA and NECA failed to reproduce the effect of adenosine, and 2-CADO enhanced the EPSCs. A1 antagonist DPCPX competitively inhibited adenosine action. A2 agonist DPMA potentiated EPSCs, and its effect was abolished by A2 antagonist DMPX. Adenosine and ATP failed to affect the nonquantal release of glutamate. The results show for the first time the presence of presynaptic adenosine receptors regulating transmitter release at insect motor nerve terminals and point to differences in pharmacological properties of adenosine receptor subtypes in insects and vertebrates.

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REFERENCES

  1. Ralevic, V. and Burnstock, G. 1998. Receptors for purines and pyrimidines. Pharm. Rev. 50:413–492.

    PubMed  Google Scholar 

  2. Fredholm, B. B., Ijzerman, A. P., Jacobson, K. A., Klotz, K.-N., and Linden, J. 2001. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharm. Rev. 53:527–552.

    PubMed  Google Scholar 

  3. Ginsborg, B. L. and Hirst, G. D. S. 1972. The effect of adenosine on the release of the transmitter from the phrenic nerve of the rat. J. Physiol. (Lond.) 224:629–645.

    Google Scholar 

  4. Fredholm, B. R. and Dunwiddie, T. V. 1988. How does adenosine inhibit transmitter release? Trends Pharmacol. Sci. 9: 130–134.

    PubMed  Google Scholar 

  5. Ribeiro, J. A., Cunha, R. A., Correia de Sa, P., and Sebastiao, A. M. 1996. Purinergic regulation of acetylcholine release. Prog. Brain Res. 109:231–241.

    PubMed  Google Scholar 

  6. Silinsky, E. M. and Redman, R. S. 1996. Synchronous release of ATP and neurotransmitter within milliseconds of a motor nerve impulse in the frog. J. Physiol. (Lond.) 492:815–822.

    Google Scholar 

  7. Tuček, S. 1990. The synthesis of acetylcholine: Twenty years of progress. Prog. Brain Res. 84:467–477.

    PubMed  Google Scholar 

  8. Lynge, J., Juel, C., and Hellsten, Y. 2001. Extracellular formation and uptake of adenosine during skeletal muscle contraction in the rat: Role of adenosine transporters. J. Physiol. (Lond.) 537:597–605.

    Google Scholar 

  9. Giniatullin, R. A. and Sokolova, E. M. 1998. ATP and adenosine inhibit transmitter release at the frog neuromuscular junction through distinct presynaptic receptors. Br. J. Pharmacol. 124:839–844.

    PubMed  Google Scholar 

  10. Inoue, K. 1998. ATP receptors for the protection of hippocampal functions. Jpn. J. Pharmacol. 78:405–410.

    PubMed  Google Scholar 

  11. Proctor, W. R. and Dunwiddie, T. V. 1987. Pre-and postsynaptic actions of adenosine in the in vitro rat hippocampus. Brain Res. 426:187–190.

    PubMed  Google Scholar 

  12. Poli, A., Lucchi, R., Vibio, M., and Barnabei, O. 1991. Adenosine and glutamate modulate each other's release from rat hippocampal synaptosomes. J. Neurochem. 57:298–306.

    PubMed  Google Scholar 

  13. Heinrich, R., Wenzel, B., and Elsner, N. 2001. A role for muscarinic excitation: Control of specific singing behavior by activation of the adenylate cyclase pathway in the brain of grasshoppers. Proc. Natl. Acad. Sci. USA 98:9919–9923.

    PubMed  Google Scholar 

  14. Parmentier, M. L., Pin, J. P., Bockaert, J., and Grau, Y. 1996. Cloning and functional expression of a Drosophila metabotropic glutamate receptor expressed in the embryonic CNS. J. Neurosci. 16:6687–6694.

    PubMed  Google Scholar 

  15. Blenau, W. and Baumann, A. 2001. Molecular and pharmacological properties of insect biogenic amine receptors: Lessons from Drosophila melanogaster and Apis mellifera. Arch. Insect Bioch. Physiol. 48:13–38.

    Google Scholar 

  16. Caruso-Neves, C., Moteiro, S. O., de Oliveria, C. F., Filho, C. C., and Lopes, A. G. 2000. Adenosine modulates the (Na++K+) ATPase activity in Malpighian tubules isolated from Rhodnius prolixus. Arch. Insect Bioch. Physiol. 43:72–77.

    Google Scholar 

  17. Mitchell, B. K. 1976. Physiology of an ATP receptor in labellar sensilla of the tsetse fly Glossina morsitans morsitans Westw. (Diptera: Glossinidae). J. Exp. Biol. 65:259–271.

    PubMed  Google Scholar 

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

    Google Scholar 

  19. Samoilova, M. V., Frolova, E. V., Potapjeva, N. N., Fedorova, I. M., Gmiro, V. E., and Magazanik, L. G. 1997. Channel blocking drugs as tools to study glutamate receptors in insect muscles and molluscan neurons. Invert. Neurosci. 3:117–126.

    Google Scholar 

  20. Kreutzberg, G. W., Heymann, D., and Reddington, M. 1986. 5′-Nucleotidase in the nervous system. Pages 149–164, in Kreutzberg, G. W., Reddington, M., and Zimmermann, H. (eds.), Cellular Biology of Ectoenzymes, Berlin, Heidelberg:Springer-Verlag.

    Google Scholar 

  21. Zimmermann, H., Braun, N., Kegel B., and Heine P. 1998. New insights into molecular structure and function of ectonucleotidases in the nervous system. Neurochem. Int. 32:421–425.

    PubMed  Google Scholar 

  22. Dunn, P. M. and Blakely, A. G. H. 1988. Suramin: A reversible P2 receptor antagonist in the mouse vas deferens. Br. J. Phar-macol. 93:243–245.

    Google Scholar 

  23. Sebastiao, A. M. and Ribeiro, J. A. 1900. Interactions between adenosine and phorbol esters or lithium at the frog neuromuscular junction. Br. J. Pharmacol. 100:55–62.

    Google Scholar 

  24. Nagano, O., Foldes, F. F., Nakatsuka, H., Reich, D., Ohta, Y., Sperlagh, B., and Vizi, E. S. 1992. Presynaptic A1-purinoceptor-mediated inhibitory effects of adenosine and its stable analogues on the mouse hemidiaphragm preparation. Naunyn Schmiedebergs Arch. Pharmacol. 346:197–202.

    PubMed  Google Scholar 

  25. Sebastiao, A. M. and Ribeiro, J. A. 1989. 1,3,8-and 1,3,7-substititted xanthines: Relative potency as adenosine receptor antagonists at the frog neuromuscular junction. Br. J. Pharmacol. 96:211–219.

    PubMed  Google Scholar 

  26. Redman, R. S. and Silinsky, E. M. 1993. A. selective adenosine antagonist (8-cyclopentyl-1,3-dipropylxanthine) eliminates both neuromuscular depression and the action of exogenous adenosine by an effect on A(1) receptors. Mol. Pharmacol. 44:835–840.

    PubMed  Google Scholar 

  27. Antonov, S. M. and Magazanik, L. G. 1988. Intense nonquantal release of glutamate in an insect neuromuscular junction. Neurosci. Lett. 93:204–208.

    PubMed  Google Scholar 

  28. Muller, D., Loctin, F., and Dunant, Y. 1987. Inhibition of evoked acetylcholine release: Two different mechanisms in the Torpedo electric organ. Eur. J. Pharmacol. 133:225–234.

    PubMed  Google Scholar 

  29. Dunwiddie, T. V. 1985. The physiological role of adenosine in the central nervous system. Int. Rev. Biochem. 27:63–139.

    Google Scholar 

  30. Haas, H. L. and Greene, R. W. 1988. Endogenous adenosine inhibits hippocampal CAl neurones: Further evidence from extra-and intracellular recording. Naunyn Schmiedebergs Arch. Pharmacol. 337:561–565.

    PubMed  Google Scholar 

  31. Scholz, K. P. and Miller, R. J. 1992. Inhibition of quantal transmitter release in the absence of calcium influx by a G-protein-linked adenosine receptor at hippocampal synapses. Neuron. 8:1139–1150.

    PubMed  Google Scholar 

  32. Haas, H. L. and Selbach, O. 2000. Functions of neuronal adenosine receptors. Naunyn Schmideberg Arch. Pharmacol. 362: 375–381.

    Google Scholar 

  33. Ribeiro, J. A. and Walker, J. 1975. The effects of adenosine triphosphate and adenosine diphosphate on transmission at the rat and frog neuromuscular junction. Br. J. Pharmacol. 54:312–318.

    Google Scholar 

  34. Silinsky, E. M. and Hirsh, J. K. 1988. The effect of reduced temperature on the inhibitory action of adenosine and magnesium on frog motor nerve terminals. Br. J. Pharmacol. 93:839–845.

    PubMed  Google Scholar 

  35. Sebastiao, A. M. and Ribeiro, J. A. 2000. Fine-tuning neuromodulation by adenosine. Trends Pharmacol. Sci. 21:341–346.

    PubMed  Google Scholar 

  36. Klinger, M., Freissmuth, M., and Nanoff, C. 2002. Adenosine receptors: G-protein-mediated signalling and the role of accessory proteins. Cell Signal. 14:99–108.

    PubMed  Google Scholar 

  37. Leaney, J. L. and Tinker, A. 2000. The role of members of the pertussis toxin-sensitive family of G-proteins in coupling receptors to the activation of the G-protein-gated inwardly rectifying potassium channel. Proc. Natl. Acad. Sci. USA 97:5651–5656.

    PubMed  Google Scholar 

  38. Chen, H. and Lambert, N. 2000. Endogenous regulators of G-protein signaling proteins regulate presynaptic inhibition at rat hippocampal synapses. Proc. Natl. Acad. Sci. USA 97:12810–12815.

    PubMed  Google Scholar 

  39. Straiker, A. J., Borden, C. R., and Sullivan, J. M. 2002. G-Protein α subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J. Neurosci. 22:2460–2468.

    PubMed  Google Scholar 

  40. Schramm, M. and Dudel, J. 2001. Pertussis toxin does not affect the time-course of quantal release in crayfish and mouse muscle, but has other post-and presynaptic effects, especially on adenosine autoreceptors. Neurosci. Lett. 299:193–196.

    PubMed  Google Scholar 

  41. Galkin, A. V., Giniatullin, R. A., Mukhtarov, M. R., Svandova, I., Grishin, S. N., and Vyskočil, F. 2001. ATP but not adenosine inhibits nonquantal acetylcholine release at the mouse neuromuscular junction. Eur. J. Neurosci. 13:2047–2053.

    PubMed  Google Scholar 

  42. Mathers, D. A. and Usherwood, P. N. R. 1976. Concanavalin A blocks desensitization of glutamate receptors on insect muscle fibres. Nature. 259:409–411.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciencesv, ???

    I. M. Fedorova

  2. Thorez pr. 44, S-Petersburg, 194223, Russia

    L. G. Magazanik & I. M. Fedorova

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  1. L. G. Magazanik
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Correspondence to L. G. Magazanik.

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Magazanik, L.G., Fedorova, I.M. Modulatory Role of Adenosine Receptors in Insect Motor Nerve Terminals. Neurochem Res 28, 617–624 (2003). https://doi.org/10.1023/A:1022893928104

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