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Guanine nucleotide-induced enhancement of affinity of dopaminergic membrane receptors of nerve tissues ofLymnaea stagnalis for agonists

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Abstract

Reception of labeled dopamine [7,83H] DA (hereafter, DA) and of a D1 receptor agonist, [3H] SKF 38393, in membranes from nerve tissues of the fresh-water lunged mollusc,Lymnaea stagnalis, was investigated. The presence of 10−6 to 10−5 M of guanine di- and triphosphate as well as of their nonhydrolizable analogs amplified the binding of agonists to membrane DA receptors, especially after EGTA addition. Replacement of EGTA with EDTA partly suppressed the binding amplification effect. Higher concentrations of guanine nucleotides (10−3 to 10−4 M) inhibited the binding of DA and of its agonists. The GDPβS-dependent stimulation of agonist binding was found not to be induced by subunits of GTP-binding proteins (G proteins), immunologically similar to β1-, β2-, and Goα-subunits of G protein in vertebrates. Membrane phosphorylation by a catalytic subunit of cAMP-dependent protein kinase fully inhibited the stimulating effect of guanine nucleotides on the agonist binding to DA receptors and markedly depressed the DA-dependent GTPase activity.

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References

  1. L. Birnbaumer, J. Abramowitz, and A. M. Brown, “Receptor-effector coupling by G proteins,”Biochim. Biophys. Acta,1031, No. 1, 163–224 (1990).

    Google Scholar 

  2. A. G. Gilman, “G proteins: transducers of receptor-generated signals,”Annu. Rev. Biochem.,56, No. 2, 615–649 (1987).

    Google Scholar 

  3. T. R. Werkman, T. A. De Vlieger, and J. C. Stoof, “Indications for a hormonal function of the snailLymnaea stagnalis,”Neurosci. Lett.,101, No. 1/2, 167–172 (1990).

    Google Scholar 

  4. T. R. Werkman, J. C. Lodder, T. A. De Vlinger, and J. C. Stoof, “Further pharmacological characterization of a D-2-line dopamine receptor on growth-hormon producing cells inLymnaea stagnalis,”Eur. J. Pharmacol.,139, No. 2, 155–161 (1987).

    Google Scholar 

  5. J. C. Stoof, T. A. De Vlieger, and J. C. Looder, “Opposing roles for D1 and D2 dopamine receptors in regulating the excitability of growth-hormone producing cells in the snailLymnaea stagnalis,”Eur. J. Pharmacol.,106, No. 2, 431–435 (1984).

    Google Scholar 

  6. T. R. Werkman, E. Schepens, T. A. De Vlienger, and J. C. Stoof, “Cyclic AMP production in the central nervous system of the snailLymnaea stagnalis is stimulated by forskolin and 5-hydroxytryptamine but is not affected by dopamine,”Comp. Biochem. Physiol. Ser. C,95, No. 2, 163–169 (1990).

    Google Scholar 

  7. I. M. Prudnikov, O. N. Osipenko, T. F. Kastrikina, and V. N. Tsyvkin, “Effect of dopamine on ionic conduction and adenylate cyclase activity in the largeLymnaea central nervous system,”Neirofiziologiya,24, No. 4, 437–451 (1992).

    Google Scholar 

  8. P. C. Sternweis and I.-H. Pang, “Mechanisms of G protein action: insight from reconstitution,” in:G Proteins and Signal Transduction, Rockefeller Univ. Press, New York (1989), pp. 197–205.

    Google Scholar 

  9. R. M. Harris-Warrick, C. Hammound, D. Paupardin-Tritch, et al., “An α40-subunit of a GTP-binding protein immunologically related to mammalian Go mediated a dopamine-induced decrease of calcium current in snail neurons,”Neuron,1, No. 1, 11–27 (1988).

    Google Scholar 

  10. I. M. Prudnikov, V. N. Tsyvkin, and T. F. Kastrikina, “GTP-dependent dopamine reception in tissues of central nervous system of the largeLymnaea,”Neirofiziologiya,24, No. 4, 451–461 (1992).

    Google Scholar 

  11. M. Bouvier, L. M. F. Leed-Londberg, J. L. Benovic, et al., “Regulation of adrenergic receptor function by phosphorylation. II. Effects of agonist occupancy on phosphorylation of α1- and β2-adrenergic receptors by protein kinase C and cyclic AMP-dependent protein kinase,”Proc. Natl. Acad. Sci. USA,262, No. 7, 3116–3125 (1987).

    Google Scholar 

  12. W. Klein, J. Sullivan, A. Scorupa, and J. S. Aguilar, “Plasticity of neuronal receptors,”FASEB J.,3, No. 5, 2132–2140 (1989).

    Google Scholar 

  13. M. Matsumoto, K. Sasaki, K. Takashima, and M. Sato, “Desensitization of dopamine receptors observed inAplysia ganglion cells,”Jpn. J. Physiol.,37, No. 2, 327–331 (1987).

    Google Scholar 

  14. H. Harada, H. Ueda, Y. Wada, et al., “Phosphorylation of μ-opioid receptors — a putative mechanism of selective uncoupling of receptor—Gi interaction, measured with low-Km GTPase and nucleotide-sensitive agonist binding,”Neurosci. Lett.,100, No. 1/3, 221–226 (1989).

    Google Scholar 

  15. Z. Elazar and S. Fushs, “Phosphorylation by cyclic AMP-dependent protein kinases modulates agonist binding to the D2 dopamine receptor,”J. Neurochem.,56, No. 1, 184–191 (1991).

    Google Scholar 

  16. T. E. Audesirk, “Characterization of pre- and post-synaptic dopamine receptors inLymnaea,”Comp. Biochem. Physiol. Ser. C,93, No. 1, 115–119 (1989).

    Google Scholar 

  17. K. S. Rózsa, “The pharmacology of molluscan neurons,”Prog. Neurobiol.,23, No. 1, 79–150 (1984).

    Google Scholar 

  18. M. Sidney and J. Gosp, Jr., “Studies of dopamine pharmacology in molluscs,”Life Sci.,33, No. 20, 1945–1959 (1983).

    Google Scholar 

  19. P. H. Andersen, J. A. Gingrich, M. D. Bates, et al., “Dopamine receptor subtypes: beyond the D1/D2 classification,”Trends Pharmacol.,11, No. 2, 231–235 (1990).

    Google Scholar 

  20. K. M. O'Boyle, D. E. Gaitanopoulos, V. Brenner, and J. L. Waddington, “Agonist and antagonist properties of benzazepine and thienopyridine derivatives at the D1 dopamine receptor,”Neuropharmacology,28, No. 4, 401–405 (1989).

    Google Scholar 

  21. B. Sutor and G. Ten Bruggencate, “Ascorbic acid: a useful reductant to avoid oxidation of catecholamines in electrophysiological experimentsin vitro,”Neurosci. Lett.,116, No. 2, 287–292 (1990).

    Google Scholar 

  22. A. E. Lant and R. Whittam, “The influence of ions on the labelling of adenosine triphosphate in red cell ghosts,”J. Physiol.,199, No. 1, 457–484 (1968).

    Google Scholar 

  23. O. H. Lowry, N. J. Rozenberg, A. L. Farr, et al., “Protein measurement with the folin phenol reagent,”J. Biol. Chem., No. 1, 265–275 (1951).

    Google Scholar 

  24. S. J. Enna, “Radioligand Binding Assays,” in:Principles and Methods in Receptor Binding, Plenum Press, NATO Sci. Affairs Div., New York; London (1989), pp. 13–32.

    Google Scholar 

  25. M. N. Pertseva, L. A. Kuznetzova, S. A. Plesneva, et al., “β-agonist-induced inhibitory-guanine-nucleotide-binding regulatory protein coupling to adenylate cyclase in molluscAnadonta cygnea foot muscle sarcolemma,”Eur. J. Biochem.,210, No. 4, 279–286 (1992).

    Google Scholar 

  26. T. Higashijima, K. M. Ferguson, P. C. Sternwels, et al., “Effects of Mg2+ and the βγ-subunit complex on the interactions of guanine nucleotides with G proteins,”J. Biol. Chem.,262, No. 2, 762–766 (1987).

    Google Scholar 

  27. P. J. Bechtel, J. A. Beavo, and E. G. Krebs, “Supplementary material to purification and characterization of the catalytic subunit from skeletal muscle adenosine 3′,5′-monophosphate-dependent protein kinase,”J. Biol. Chem.,252, No. 8, 2691–2697 (1977).

    Google Scholar 

  28. S. Endo, S. Shenolikar, A. Eskin, et al., “Characterization of neuronal protein phosphatases inAplysia californica,”J. Neurochem.,58, No. 3, 972–975 (1992).

    Google Scholar 

  29. J. C. Stoof and J. W. Kebabian, “Opposing roles for D1 and D2 dopamine receptors in efflux of cyclic AMP from rat neostriatum,”Nature,294, No. 2333, 366–368 (1981).

    Google Scholar 

  30. A. Sidhu, M. Sullivan, T. Kohout, et al., “D1 dopamine receptors can interact with both stimulatory and inhibitory guanine nucleotide binding proteins,”J. Neurochem.,57, No. 4, 1445–1451 (1991).

    Google Scholar 

  31. S. E. Senogles, A. M. Spiegel, E. Padrell, et al., “Specificity of receptor—G protein interactions,”J. Biol. Chem.,265, No. 8, 4507–4514 (1990).

    Google Scholar 

  32. C. C. Felder, P. A. Jose, and J. Axelrod, “The dopamine-1 agonist, SKF 82526, stimulates phospholipase C activity independent of adenylate cyclase,”J. Pharmacol. Exp. Ther.,248, No. 1, 45–56 (1989).

    Google Scholar 

  33. P. M. Lledo, V. Homburger, and J. Bockert, “Differential G protein-mediated coupling of D2 dopamine receptors to K+ and Ca+ currents in rat anterior pituitary cells,”Neuron,8, No. 3, 455–463 (1992).

    Google Scholar 

  34. P. Deterre, D. Paupardin-Tritch, and J. Bockaert, “Serotonin and dopamine sensitive adenylate cyclase in molluscan nervous system. Biochemical and electrophysiological analysis of the pharmacological properties and the GTP-dependence,”Mol. Brain Res.,1, No. 1, 101–109 (1986).

    Google Scholar 

  35. A. H. Drummond, F. Bucher, and I. V. Levitan, “Distribution of serotonin and dopamine receptors inAplysia tissues: analysis (3H)-LSD binding and adenylate cyclase stimulation,”Brain Res.,184, No. 1, 163–177 (1980).

    Google Scholar 

  36. A. H. Drummond, F. Bucher, and I. V. Levitan, “d-[3H] lysergic acid diethylamide binding to serotonin receptors in the molluscan nervous system,”J. Biol. Chem.,255, No. 14, 6679–6686 (1980).

    Google Scholar 

  37. M. H. Makman, I. Berrios, S. Pratt, et al., “Anatomical localization of dopaminergic systems inOctopus retina: evidence for intrinsic dopamine-containing cells and dopamine D1 receptors,” in:Neurobiology Molluscan Models, Proc. Sec. Symp. Mollusc. Neurobiol., Amsterdam (1986), pp. 31–35.

  38. T. Watanabe, K. Umegaki, and W. L. Smath, “Association of a solubilized prostaglandin E2 receptor from renal medulla with a pertussis toxin-reactive guanine nucleotide regulatory protein,”J. Biol. Chem.,261, No. 29, 13430–13439 (1986).

    Google Scholar 

  39. S. S. Taylor, “cAMP-dependent protein kinase,”J. Biol. Chem.,264, No. 8, 8443–8446 (1989).

    Google Scholar 

  40. M. Bushfield, G. J. Murphy, B. E. Lavan, et al., “Hormonal regulation of Gi2α-subunit phosphorylation in intact hepatocytes,”Biochem. J.,268, No. 2, 449–457 (1990).

    Google Scholar 

  41. K. Haga and T. Haga, “Dual regulation by G protein of agonist-dependent phosphorylation of muscarinic acetylcholine receptors,”FEBS,268, No. 1, 43–47 (1990).

    Google Scholar 

  42. H. Morii, M. Tanemura, and Y. Watanabe, “Regulation of prostaglandin E2 receptor binding activity in porcine temporal cortex by protein phosphorylation,”J. Neurochem.,57, No. 4, 1281–1295 (1991).

    Google Scholar 

  43. J. L. Benovic, J. J. Onorato, and M. J. Caron, “Regulation of G protein coupled receptors by agonist-dependent phosphorylation,” in:G Proteins and Signal Transduction, Rockefeller Univ. Press, New York (1989), pp. 87–103.

    Google Scholar 

  44. Y. Watanabe, T. Imaizumi, N. Misaki, et al., “Effects of phosphorylation of inhibitory GTF-binding protein by cyclic AMP-dependent protein kinase on its ADP — ribosylation by pertussis toxin, islet activating protein,”FEBS,236, No. 2, 372–374 (1988).

    Google Scholar 

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Neirofiziologiya/Neurophysiology, Vol. 25, No. 5, pp. 334–343, September–October, 1993.

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Prudnikov, I.M. Guanine nucleotide-induced enhancement of affinity of dopaminergic membrane receptors of nerve tissues ofLymnaea stagnalis for agonists. Neurophysiology 25, 271–278 (1993). https://doi.org/10.1007/BF01054257

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