Skip to main content
SpringerLink
Log in

Comparative aspects of opioid-dopamine interaction

  • Review and Commentary
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Summary

  1. 1.

    Opiate receptors are found in invertebrate as well as mammalian systems, often in proximity to dopamergic systems. This review summarizes the interrelationships between these two transmitter systems in invertebrates.

  2. 2.

    The comparative data discussed here are of considerable significance. They recall that the opioid-dopamine relationships first demonstrated in the mammalian nervous system also apply to invertebrates and are therefore of more general importance. The results obtained in the molluskMytilus strengthen the concept that the activity of dopaminergic neurons may be modulated by afferent opioid signals and that, even in “more primitive” animals, interneuronal transfer of information is more complex than formerly visualized. Furthermore, the data indicate that endogenous opioids may exert tonic control over dopamine metabolism, thus implying interdependence of the two systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arbilla, S., and Langer, S. Z. (1978). Morphine and B-endorphin inhibit release of noradrenaline from cerebral cortex but not of dopamine from rat striatum.Nature 271559–561.

    Google Scholar 

  • Atweh, S. F., Murin, L. C., and Kuhar, M. J. (1978). Presynaptic localization of opiate receptors in the vagal and accessory optic systems: An autoradiographic study.Neuropharmacology 1765–71.

    Google Scholar 

  • Biggio, G., Casu, M., Corda, M. G., DiBello, C., and Gersa, G. L. (1978). Stimulation of dopamine synthesis in caudate nucleus by intrastriatal enkephalins and antagonism by naloxone.Science 200552–554.

    Google Scholar 

  • Bloom, F., Battenberg, E., Rossier, J., Ling, N., and Guillemin, R. (1978). Neurons containing B-endorphin in rat brain exist separately from those containing enkephalin: Immunocytochemical studies.Proc. Natl. Acad. Sci. 751591–1595.

    Google Scholar 

  • Burrell, D. E., and Stefano, G. B. (1982). Analysis of monoamine accumulation in the neuronal tissues of Mytilus edulis (Bivalvia). IV. Variations due to age.Comp. Biochem. Physiol. (in press).

  • Carenzi, A., Guidotti, A., Revvelta, A., and Costa, E. (1975). Molecular mechanisms in the actions of morphine and viminol (R2) on rat striatum.J. Pharmacol. Exp. Ther. 194311–318.

    Google Scholar 

  • Clouet, D. H., and Iwatsubo, K. (1975). Dopamine-sensitive adenylate cyclase of the caudate nucleus of rats treated with morphine.Life Sci. 1735–40.

    Google Scholar 

  • Codd, E. E., and Byrne, W. L. (1980). Seasonal variation in the apparent number of H-naloxone binding sites. InEndogenous and Exogenous Opiate Agonists and Antagonists (Way, E. L., Ed.), Pergamon Press, New York, pp. 63–66.

    Google Scholar 

  • Costall, B., and Naylor, R. J. (1973). Neuroleptic and non-neuroleptic catalepsy.Anzmeim-Forsch. 23674–683.

    Google Scholar 

  • Davis, G. C., Bunney, W. E., DeFraites, E. G., Kleinman, J. E., van Kammen, D. P., Post, R. M., and Wyatt, R. J. (1977). Intravenous naloxone administration in schizophrenic and affective illness.Science 19774.

    Google Scholar 

  • Deyo, S., Swift, R., and Miller, R. J. (1979). Morphine and endorphins modulate dopamine turnover in rat median eminence.Proc. Natl. Acad. Sci. 774341–4344.

    Google Scholar 

  • Eidelberg, E., and Erspamer, J. (1975). Dopaminergic mechanisms of opiate actions in the brain.J. Pharmacol. Exp. Ther. 19250–57.

    Google Scholar 

  • Ferland, L., Fuxe, K., Feroch, P., Gustafssen, J. B., and Skelt, P. (1977). Effects of methionine-enkephalin on prolactin release and catecholamine levels and turnover in the median eminence.Eur. J. Pharmacol. 4389–94.

    Google Scholar 

  • Finch, C. E., Potter, D. E., and Kenny, A. D., (Ed.) (1978).Adv. Exp. Med. Biol. 113.

  • Forn, J., Krueger, B. K., and Greengard, S. P. (1974). Adenosine 3′,5′ monophosphate content in rat caudate nucleus: Demonstration of dopaminergic and adrenergic receptors.Science 1861118–1120.

    Google Scholar 

  • Frederickson, R. C. A., Mickander, R., Smithwick, E. L., Shuman, R., and Morris, F. H. (1976). Pharmacological activity of Met. enkephalin and analogues in vitro and in vivo depression of single neuronal activity in specified brain regions. InOpiates and Endogenous Opioid Peptides, Elsevier/North-Holland, Amsterdam.

    Google Scholar 

  • Gardner, E. L., Mishra, R. K., Iordanidis, P., Katzman, R., and Makman, M. H. (1976). Catalytic and receptor components of enhanced dopamine-stimulated adenylate cyclase in two behaviorally distinct striatal denervation syndromes.Fed. Proc. 35456.

    Google Scholar 

  • Gardner, E. L., Zukin, R. S., and Makman, M. H. (1980). Modulation of opiate receptor binding in striatum and amygdala by selective mesencephalic lesions.Brain Res. 194232–239.

    Google Scholar 

  • Gauchy, C., Acid, T., Glowinski, J., and Cheramy, A. (1973). Acute effects of morphine on dopamine synthesis and release and tyrosine metabolism in the rat striatum.Eur. J. Pharmacol. 22311–319.

    Google Scholar 

  • Hess, G. D., Joseph, J. A., and Roth, G. S. (1981). Effect of age on sensitivity to pain and brain opiate receptors.Neurobiol. Aging 249–55.

    Google Scholar 

  • Hill, R., Pepper, C. M., and Mit, I. F. (1976). The repressant action of iontophoretically applied met. enkephalin on a single neuron in rat.Nature 262604–605.

    Google Scholar 

  • Hokfelt, T., Ljungdahl, A., Terenius, L., Elde, R., and Wilsson, G. (1977). Immunohistochemical analysis of peptide pathways possibly related to pain and analgesia: Enkephalin and substance P.Proc. Natl. Acad. Sci. 743081–3085.

    Google Scholar 

  • Hong, J. S., Tang, H. Y., Fratta, W., and Costa, E. (1977). Determination of Met. enkephalin in discrete regions of rat brain.Brain. Res. 134383–386.

    Google Scholar 

  • Hughes, J., Kosterlitz, N. H., and Leslie, F. M. (1975). Effects of morphine on adrenergic transmission in the mouse vas deferens. Assessment of agonist and antagonist potencies of narcotic analgesics.Br. J. Pharmacol. 53371.

    Google Scholar 

  • Iwatsubo, K., and Clouet, D. H. (1975). Dopamine-sensitive adenylate cyclase of the caudate nucleus of rats treated with morphine or haloperidol.Biochem. Pharmacol. 141499–1503.

    Google Scholar 

  • Jessell, T. M., and Iversen, L. L. (1977). Opiate analgesics inhibit substance P release from rat trigeminal nerve.Nature 268549–551.

    Google Scholar 

  • Jhamandas, K., Sawynok, J., and Sutak, M. (1977). Enkephalin effects on release of brain acetylcholine.Nature 269433–435.

    Google Scholar 

  • Kebabian, J. W., and Calne, D. B. (1979). Multiple receptors for dopamine.Nature 27793–96.

    Google Scholar 

  • Kebabian, J. W., and Saavedra, J. M. (1976). Dopamine-sensitive adenylate cyclase occurs in a region of substantia nigra containing dopaminergic dentrites.Science 193683–685.

    Google Scholar 

  • Kobayashi, R., Palkovits, M., Miller, R. J., Chang, K. J., and Cautrecases, P. (1978). Hypophysectomy does not alter rat brain enkephalin distribution.Life Sci. 22379–389.

    Google Scholar 

  • Kream, R. M., and Zukin, R. S. (1979). Binding characteristics of a potent enkephalin analog.Biochem. Biophys. Res. Commun. 9099–109.

    Google Scholar 

  • Kream, R. M., Zukin, R. S., and Stefano, G. B. (1980). Demonstration of two classes of opiate binding sites in the nervous tissue of the marine mollusc Mytilus edulis: Positive homotropic cooperativity of lower affinity binding sites.J. Biol. Chem. 225(19):9218–9224.

    Google Scholar 

  • Kuhar, M. J., Pert, C. B., and Snyder, S. H. (1973). Regional distribution of opiate receptors binding in monkey and human brain.Nature 245447–450.

    Google Scholar 

  • Kuschinsky, K. (1976). Actions of narcotics on brain dopamine metabolism and their relevance for “psychomotor” effects.Arzneim-Forsch. 26563–567.

    Google Scholar 

  • Lal, H. (1975). Narcotic dependence, narcotic action and dopamine receptors.Life Sci. 17483–496.

    Google Scholar 

  • Lamotte, C., Pert, C. B., and Snyder, S. H. (1976). Opiate receptor binding in primate spinal cord: Distribution and changes after dorsal section.Brain Res. 112567–568.

    Google Scholar 

  • Loh, H. H., Brase, D. A., Sampathe-Khanna, S., Mar, J. B., and Way, E. L. (1976). B-Endorphin in vitro inhibition of striatal dopamine release.Nature 264567–568.

    Google Scholar 

  • Lord, J. A. H., Waterfield, A. A., Hughes, J., and Kosterlitz, H. W. (1976). Multiple opiate receptors. InOpiates and Endogenous Opioid Peptides, (Kosterlitz, H. W., Ed.), Elsevier/North-Holland, Amsterdam, pp. 275–280.

    Google Scholar 

  • Malanga, C. J., Poll, K. A., and O'Donnell, J. P. (1980). Agonist and antagonist effects of dopaminergic stimulation of cAMP in the ciliated cell epithelium of the marine mussel Mytilus edulis.Fed. Proc. 39(3):abstr. 3179.

    Google Scholar 

  • Maldonado, H., and Miralto, A. (1982). Effect of morphine and naloxone on a defensive response of the mantis shrimp.J. Comp. Physiol. (in press).

  • Messing, R. B., Vasquez, B. J., Spiehber, V. R., Martinez, J. L., Jensen, R. A., Ritger, H., and McGaugh, J. L. (1980).3H-Dihydromorphine binding in brain regions of young and aged rats.Life Sci. 26921–927.

    Google Scholar 

  • Messing, R. B., Vasquez, B. J., Samamiego, B., Jensen, R. A., Martinez, J. L., and McGaugh, J. L. (1981). Alterations in dihydromorphine binding in cerebral hemispheres of aged male rats.J. Neurochem. 36784–790.

    Google Scholar 

  • Miller, R. J., and Pickel, V. M. (1980). Immunohistochemical distribution of enkephalins: Interactions with catecholamine-containing systems. InHistochemistry of Cell Biology of Autonomic Neurons, SIF Cells and Paraneurons (Eranko, E., Ed.), Raven Press, New York, pp. 349–359.

    Google Scholar 

  • Miller, R. J., Horn, A. S., and Iversen, L. L. (1974). The action of neuroleptic drugs on dopamine-stimulated adenosine cyclic 3′,5′-monophosphate production in rat neostriatum and limbic fore-brain.Mol. Pharmacol. 10759–766.

    Google Scholar 

  • Moore, R. Y., and Bloom, F. E. (1978). Central catecholamine neuron systems: Anatomy and physiology of dopamine systems.Annu. Rev. Neurosci. 1129–169.

    Google Scholar 

  • Mudge, A. W., Leeman, S. E., and Fischbach, G. D. (1979). Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration.Proc. Natl. Acad. Sci. 76526.

    Google Scholar 

  • Osborne, N. N., and Neuhoff, V. (1979). Are there opiate receptors in the invertebrates?J. Pharm. Pharmacol. 31481.

    Google Scholar 

  • Pollard, H., Llorens, C., Bonnet, J. J., Costentin, J., and Schwartz, J. C. (1977a). Opiate receptors on mesolimbic dopaminergic neurons.Neurosci. Lett. 7295–299.

    Google Scholar 

  • Pollard, H., Llorens-Cortes, C., and Schwartz, J. C. (1977b). Enkephalin receptors on dopaminergic neurons in rat striatum.Nature 268745.

    Google Scholar 

  • Pollard, H., Llorens, C., Schwartz, J. C., Gros, C., and Dray, F. (1978). Localization of opiate receptors and enkephalins in the rat striatum in relationship with the nigrostriatal dopaminergic system: Lesion studies.Brain. Res. 151392–398.

    Google Scholar 

  • Puri, S. K., Cochin, J., and Volicer, L. (1975). Effect of morphine sulfate on adenylate cyclase and phosphodiesterase activity in rat corpus striatum.Life Sci. 16759–767.

    Google Scholar 

  • Saanivaara, L. (1969). Analgesic activity of some sympathetic drugs and their effect on morphine analgesia in rabbits.Ann. Med. Exp. Biol. Fenn. 47180–190.

    Google Scholar 

  • Sar, N., Stumpf, W. E., Miller, R. J., Chang, K. J., and Catrecases, P. (1978). Immunohistochemical localization of enkephalin in rat brain and spinal cord.J. Comp. Neurol. 18217–38.

    Google Scholar 

  • Satoh, M., Akaike, A., and Takagi, H. (1979). Excitation by morphine and enkephalin of single neurons of nucleus reticularis paragigantocellularis in the rat: A probable mechanism of analgesic action of opioids.Brain Res. 169406–410.

    Google Scholar 

  • Schaumann, W. (1957). Inhibition by morphine of the release of acetylcholine from the intestine of the guinea-pig.Br. J. Pharmacol. 12115–120.

    Google Scholar 

  • Simantov, R., Kuhar, M. J., Whl, G. R., and Snyder, S. H. (1977). Opioid peptide enkephalin immunohistochemical mapping in rat central nervous system.Proc. Natl. Acad. Sci. 742167–2171.

    Google Scholar 

  • Simon, E. J., Hiller, J. M., Groth, J., and Edelman, I. (1975). For the properties of stereospecific opiate binding in rat brain: On the nature of the sodium effect.J. Pharmacol. Exp. Ther. 192531–537.

    Google Scholar 

  • Stefano, G. B. (1981). Decrease in the number of high affinity opiate binding sites during the aging process in Mytilus edulis (Bivalvia).Cell. Mol. Neurobiol. 4343–350.

    Google Scholar 

  • Stefano, G. B. (1982). Aging: Variation in opiate binding characteristics and dopamine responsiveness in subtidal and intertidal Mytilus edulis visceral ganglia.Comp. Biochem. Physiol. 72C349–352.

    Google Scholar 

  • Stefano, G. B., and Catapane, E. J. (1977). The effects of temperature acclimation on monoamine metabolism.J. Pharmacol. Exp. Ther. 203449–546.

    Google Scholar 

  • Stefano, G. B., and Catapane, E. J. (1978). Methionine enkephalin increases dopamine levels.Soc. Neurosci. Abstr. 4283.

    Google Scholar 

  • Stefano, G. B., and Catapane, E. J. (1979). Enkephalins increase dopamine levels in the CNS of a marine mollusc.Life Sci. 241617–1622.

    Google Scholar 

  • Stefano, G. B., and Hiripi, L. (1979). Methionine enkephalin and morphine alter monoamine and cyclic nucleotide levels in the cerebral ganglia of the freshwater bivalve, Anodonta cygnea.Life Sci. 25291–298.

    Google Scholar 

  • Stefano, G. B., and Scharrer, B. (1981). High affinity binding of an enkephalin analog in the cerebral ganglion of the insect Leucophaea maderae (Blattaria).Brain Res. 225107–114.

    Google Scholar 

  • Stefano, G. B., Catapane, E. J., and Aiello, E. (1976). Dopaminergic agents influence serotonin in molluscan nervous system.Science 194539–541.

    Google Scholar 

  • Stefano, G. B., Hiripi, L., and Catapane, E. J. (1978). The effect of short- and long-term temperature stress on serotonin, dopamine, and norepinephrine metabolism in molluscan ganglia.J. Theor. Biol. 379–83.

    Google Scholar 

  • Stefano, G. B., Vadasz, I., and Hiripi, L. (1979). Naloxone selectively blocks dopamine response of Br-type neurone in Helix pomatia.Experientia 351337–1338.

    Google Scholar 

  • Stefano, G. B., Hiripi, L., Rozsa, S., and Salanki, J. (1980a). Behavioral effects of morphine on the land snail Helix pomatia: Demonstration of tolerance InNeurobiology of Invertebrates—Mechanisms and Intergration (Salonki, J., Ed.), Adv. Physiol. Sci. Vol. 23, Pergamon Press, New York, pp. 285–295.

    Google Scholar 

  • Stefano, G. B., Kream, R. M., and Zukin, R. S. (1980b). Demonstration of stereospecific opiate binding in the nervous tissue of the marine mollusc Mytilus edulis.Brain Res. 181445–450.

    Google Scholar 

  • Stefano, G. B., Kream, R. M., Zukin, R. S., and Catapane, E. J. (1980c). Seasonal variation of stereospecific enkephalin binding and dopamine responsiveness in Mytilus edulis pedal ganglia. InNeurotransmitters in Invertebrates (Rozsa, K. S., Ed.), Adv. Physiol. Sci. Vol 22, Pergamon Press, London, pp. 453–459.

    Google Scholar 

  • Stefano, G. B., Rozsa, K. S., and Hiripi, L. (1980d). Actions of methionine enkephalin and morphine on single neuronal activity in Helix pomatia.Comp. Biochem. Physiol. 66C193–198.

    Google Scholar 

  • Stefano, G. B., Vadasz, I., and Hiripi, L. (1980e). Methionine enkephalin inhibits the bursting activity of the Br-type neuron in Helix pomatia.Experientia 36666–667.

    Google Scholar 

  • Stefano, G. B., Catapane, E. J., and Kream, R. M. (1981a). Characterization of the dopamine-stimulated adenylate cyclase in the pedal ganglia ofMytilus edulis: Interactions with etorphine,β-endorphin, DALA, and methionine enkephalin.Cell. Mol. Neurobiol. 157–68.

    Google Scholar 

  • Stefano, G. B., Hall, B., Makman, M. H., and Dvorkin, B. (1981b). Opioids inhibit potassium-stimulated dopamine release in the marine mussel Mytilus edulis and in the cephalopod Octopus bimaculatus.Science 213928–930.

    Google Scholar 

  • Stefano, G. B., Scharrer, B., and Assanah, P. (1983). Demonstration, characterization and localization of opioid binding sites in the midgut of the insect Leucophaea maderae.Brain Res. (in press)

  • Stefano, G. B., Zukin, R. S., and Kream, R. M. (1981c). Tentative identification of affinity of high affinity opioid binding sites in the pedal ganglia of the marine mussel Mytilus edulis. InAdvances in Endogenous and Exogenous Opioids (Takagi, H., and Simon E. J., Eds.) Elsevier, New York, pp. 48–50.

    Google Scholar 

  • Stefano, G. B., Zukin, R. S., and Kream, R. M. (1982). Evidence for the presynaptic localization of a high affinity opiate binding site on dopamine neurons in the pedal ganglia of M. edulis (Bivalvia).J. Pharmacol. Exp. Ther. (in press)

  • Subramanian, N., Mitznegg, P., Sprugel, W., Domschke, W., Domschke, S., Wunsch, E., and Demling, L. (1977). Influence of enkephalin on K+-evoked efflux of putative neurotransmitters in rat brain.Naunyn-Schmiedeberg Arch. Pharmacol. 299163.

    Google Scholar 

  • Terry, R. D., and Gershon, S. (1976).Neurobiology of Aging, Raven Press, New York, Vol. 3.

    Google Scholar 

  • Venturini, G., Carolei, A., Palladini, G., Margotta, V., and Cerbo, R. (1981). Naloxone enhances cAMP levels in Planaria.Comp. Biochem. Physiol. 69c105–108.

    Google Scholar 

  • Walczak, S. A., Wilkening, D., and Makman, M. H. (1979). Interaction of morphine, etorphine and enkephalins with dopamine-stimulated adenylate cyclase of monkey amygdala.Brain Res. 160106–116.

    Google Scholar 

  • Wilkening, D., Mishra, R. K., and Makman, M. H. (1976). Effects of morphine on dopamine-stimulated adenylate cyclase and on cyclic GMP formation in primate brain amygdalaloid nucleus.Life Sci. 191129–1138.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, State University of New York College at Old Westbury, 11568, Old Westbury, New York, USA

    George B. Stefano

Authors
  1. George B. Stefano
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stefano, G.B. Comparative aspects of opioid-dopamine interaction. Cell Mol Neurobiol 2, 167–178 (1982). https://doi.org/10.1007/BF00711145

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00711145

Key words

Search

Navigation