Summary
Dopamine, which is present in nerve-rich tissues of the hydromedusa Polyorchis penicillatus, produces membrane hyperpolarization in identified motor neurons from this jellyfish. In this study we demonstrate that the inhibitory action of dopamine is mediated by conventional drug-receptor interactions which are reversible, saturable and specific. When 10 μM dopamine was applied by micro-spritzing onto voltage-clamped (holding potential, −20 mV), cultured “swimming” motor neurons, an outward current of about 1 nA was evoked. Using this technique, we established a potency order for several amines: dopamine≫norepinephrine>tyramine >octopamine>β-phenylethylamine. Dopamine is effective at concentrations betweeen 1 × 10-8 and 1 × 10-3 M. Several dopamine receptor blockers such as fluphenazine, haloperidol and spiperone reduced the dopamine-induced current in a concentration-dependent manner. Although propranolol, a β-adrenergic blocker, reduced the dopamine response and SKF 83566, a D1 blocker, increased the response, it appears that the dopamine receptors in these jellyfish neurons share pharmacological properties with mammalian D2 dopamine receptors.
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References
Anctil M (1989) The antiquity of monoaminergic neurotransmitters: Evidence from Cnidaria. In: Anderson PAV (ed) Evolution of the first nervous systems. Plenum Press, New York, pp 141–156
Anderson PAV (1985) Physiology of a bidirectional, excitatory, chemical synapse. J Neurophysiol 53:821–835
Anderson PAV, Grunert U (1988) Three-dimensional structure of bidirectional, excitatory chemical synapses in the jellyfish Cyanea capillata. Synapse 2:606–613
Anderson PAV, Trapido-Rosenthal HG (1990) Electrophysiological evidence that a taurine-like amino acid is the neurotransmitter at a fast excitatory synapse. Soc Neurosci Abstr 16:1185
Audesirk TE (1989) Characterization of pre- and postsynaptic dopamine receptors in Lymnaea. Comp Biochem Physiol 93C:115–119
Barger G, Dale HH (1910) Chemical structure and sympathomimetic action of amines. J Physiol (Lond) 41:19–59
Bokisch AJ, Walker RJ (1986) Properties of dopamine receptors of identified neurones in the brain of the gastropod mollusc, Helix aspersa. In: Winlow W, Markstein R (eds) The neurobiology of dopamine systems. Manchester Univ Press, UK, pp 108–111
Bullock TH (1943) Neuromuscular facilitation in Scyphomedusae. J Cell Comp Physiol 22:251–272
Chung JM, Spencer AN (1991) Dopamine as a neuroactive substance in the jellyfish Polyorchis penicillatus. J Exp Biol 156:433–451
Chung JM, Spencer AN, Gahm KH (1989) Dopamine in tissues of the hydrozoan jellyfish Polyorchis penicillatus as revealed by HPLC and GC/MS. J Comp Physiol B 159:173–181
Cooper JR, Bloom FE, Roth RH (1986) The biochemical basis of neuropharmacology. Oxford New York
Feltz A, Trautmann A (1982) Desensitization at the frog neuromuscular junction: a biphasic process. J Physiol (Lond) 322:257–272
Fenwick EM, Marty A, Neher E (1982) A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J Physiol (Lond) 331:577–597
Gero A (1983) Desensitization, two-state receptors and pharmacological parameters. J Theor Biol 103:137–161
Ginsborg BL, House CR, Silinsky EM (1976) On the receptors which mediate the hyperpolarization of salivary gland cells of Nauphoeta cinerea Olivier. J Physiol (Lond) 262:489–500
Grimmelikhuijzen CJP, Graff D, Koizumi O, Westfall JA, McFarlane ID (1989) Neurons and their peptide transmitters in coelenterates. In: Anderson PAV (ed) Evolution of the first nervous systems. Plenum Press, New York, pp 95–110
Hanai K, Kitajima M (1984) Two types of surface amine receptors modulating the feeding response in Hydra japonica: the depressing action of dopamine and related amines. Chem Senses 9:355–368
Harden TK (1983) Agonist-induced desensitization of the beta adrenergic receptor-linked adenylate cyclase. Pharmacol Rev 35:5–32
Heiss WD, Hoyer J, Thalhammer G (1976) Antipsychotic drugs and dopamine-mediated responses in Aplysia neurons. J Neural Transm 39:187–208
House CR, Ginsborg BL (1976) Action of dopamine analogue and a neuroleptic at a neuroglandular synapse. Nature 261:332–333
Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325:529–531
Jones SB, Bylund DB (1988) Characterization and possible mechanisms of α2-adrenergic receptor-mediated sensitization of forskolin-stimulated cyclic AMP production in HT 29 cells. J Biol Chem 263:14236–14244
Kahn CR (1976) Membrane receptors for hormones and neurotransmitters. J Cell Biol 70:261–286
Katz B, Thesleff S (1957) A study of the “desensitization” produced by acetylcholine at the motor end-plate. J Physiol (Lond) 138:63–80
Kenakin TP (1984) The classification of drugs and drug receptors in isolated tissues. Pharmacol Rev 36:165–222
Laduron PM (1984) Criteria for receptor sites in binding studies. Biochem Pharmacol 33:833–899
Martin SM, Spencer AN (1983) Neurotransmitters in coelenterates. Comp Biochem Physiol 74C:1–14
Paton WDM (1961) A theory of drug action based on the rate of drug-receptor combination. Proc R Soc Lond B 154:21–69
Przysiezniak J, Spencer AN (1989) Primary culture of identified neurons from a cnidarian. J Exp Biol 142:97–113
Roberts A, Mackie GO (1980) The giant axon escape system of a hydrozoan medusa, Aglantha digitale. J Exp Biol 84:303–318
Sakai M, Swartz BE, Woody CD (1979) Controlled micro release of pharmacological agents: Measurements of volume ejected in vitro through fine tipped glass microelectrodes by pressure. Neuropharmacol 18:209–213
Seeman P (1981) Brain dopamine receptors. Pharmacol Rev 32:229–313
Sibley DR, Lefkowitz RJ (1987) Beta-adrenergic receptor coupled adenylate cyclase. Mol Neurobiol 1:121–154
Singla C (1978) Fine structure of the neuromuscular system of Polyorchis penicillatus (Hydromedusae, Cnidaria). Cell Tissue Res 193:163–174
Spencer AN (1979) Neurobiology of Polyorchis. II. Structure of effector systems. J Neurobiol 10:94–117
Spencer AN (1989) Neuropeptides in the Cnidaria. Amer Zool 29:1213–1225
Spencer AN, Arkett SA (1984) Radial symmetry and the organization of central neurones in a hydrozoan jellyfish. J Exp Biol 110:69–90
Strange PG (1990) Aspects of the structure of the D2 dopamine receptor. Trans Neural Sci 13:373–378
Van Marle J (1989) Catecholamines, related compounds and the nervous system in the tentacles of some anthozoans. In: Anderson (ed) Evolution of the first nervous systems. Plenum Press, New York, pp 129–140
Werkman TR, Lodder JC,De Vlieger TA, Stoof JC (1987) Further pharmacological characterization of a D-2-like dopamine receptor on growth hormone producing cells in Lymnaea stagnalis. Eur J Pharmacol 139:155–161
Westfall JA (1987) Ultrastructure of invertebrate synapses. In: Ali MA (ed) Nervous systems in invertebrates. Plenum Press, New York London, pp 3–28
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Chung, Jm., Spencer, A.N. Dopamine acts through a D2-like receptor on a jellyfish motor neuron. J Comp Physiol A 169, 599–606 (1991). https://doi.org/10.1007/BF00193549
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DOI: https://doi.org/10.1007/BF00193549