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Invertebrate and vertebrate neuroimmune and autoimmunoregulatory commonalties involving opioid peptides

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Summary

  1. 1.

    Evidence for bidirectional interrelationships between the nervous system and immune systems of vertebrates and invertebrates involving opioid peptides is briefly discussed.

  2. 2.

    The involvement of opioid peptides in autoimmunoregulatory communication also is discussed.

  3. 3.

    The presence of mammalian interleukin-like (1 & 6) and tumor necrosis factor-like molecules in invertebrates is reviewed as well as an apparent cascading system for these signal molecules.

  4. 4.

    The significance of ACTH and MSH in cellular immunosuppression and autoimmunoregulation is discussed in the context of a potential role in schistosomiasis and human immunodeficiency virus actions.

  5. 5.

    The review concludes with the hypothesis that the mammalian immune system has its origin in the invertebrate immune/defense system given the many similarities noted in the review based on new knowledge about the more “primitive” system.

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References

  • Beck, G., and Habicht, G. S. (1986). Isolation and characterization of a primitive interleukin-1 like protein from an invertebrate, Asterias forbesi.Proc. Natl. Acad. Sci. USA 837429–7433.

    Google Scholar 

  • Beck, G., Vasta, G. R., Marchalonis, J. J., and Habicht, G. S. (1989). Characterization of interleukin-1 activity in tunicates.Comp. Biochem. Physiol. 9293–98.

    Google Scholar 

  • Brown, S. L., and Van Epps, D. E. (1985). Suppression ofT-Iymphocyte chemotactic factor production by the opioid peptides beta-endorphin and Met-enkephalin.J. Immunol. 1343384–3388.

    Google Scholar 

  • Brown, S. L., Tokuda, S., Saland, L. C., and Van Epps, D. E. (1986). Opioid peptide effects on leukocyte migration. InEnkephalins and Endorphins Stress and the Immune System (N. P. Plotnikoff, R. E. Faith, A. J. Murgo, and R. Good, Eds.), Plenum Press, New York, pp. 367–386.

    Google Scholar 

  • Committee on Models for Biomedical Research (1985).Models for Biomedical Research: A New Perspective, Natl. Acad. Sci. Press, Washington, D.C.

    Google Scholar 

  • Donnelly, J. J., Vogel, S. N., and Prendergast, R. A. (1983). Down-regulation of Ia expression on macrophages by sea star factor.Cell. Immunol. 90408–415.

    Google Scholar 

  • Duvaux-Miret, O., Stefano, G. B., Smith, E. M., Dissous, C., and Capron, A. (1991). Immunosuppression in the definitive and intermediate hosts of the human parasiteSchistosoma mansoni by release of immunoactive neuropeptides.Proc. Natl. Acad. Sci. USA 89778–781.

    Google Scholar 

  • Falke, N. E., and Fischer, E. G. (1985). Cell shape of polymorphonuclear leukocytes is influenced by opioids.Immunobiology 169532–539.

    Google Scholar 

  • Falke, N. E., and Fischer, E. G. (1986). Opiate receptor mediated internalization of 125 I-β-endorphin in human polymorphonuclear leucocytes.Cell Biol. Int. Rep. 10429–437.

    Google Scholar 

  • Falke, N. E., Fischer, E. G., and Martin, R. (1985). Stereospecific opiate binding in living human polymorphonuclear leukocytes.Cell Biol. Int. Rep. 91041–1047.

    Google Scholar 

  • Fischer, E. G., and Falke, N. E. (1984).β-Endorphin modulates immune functions—A review.Psychother. Psychosom. 42195–204.

    Google Scholar 

  • Fischer, E. G., and Falke, N. E. (1986). The influence of endogenous opioid peptides on venous granulocytes. InEnkephalins and Endorphins Stress and the Immune System (N. P. Plotnikoff, R. E. Faith, A. J. Murgo, and R. Good, Eds.), Plenum Press, New York, pp. 263–270.

    Google Scholar 

  • Horikawa, S., Takai, T., Toyosato, M., Takahashi, H., Noda, M., Kakidani, H., Kubo, T., Hirose, T., Inayama, S., Miyata, T., and Numa, S. (1983). Primary structures of B-and-S subunit precursors of Torpedo californica acetylcholine receptor deduced from cDNA sequences.Nature 306611–614.

    Google Scholar 

  • Hughes, T. K., Jr., Smith, E. M., Cadet, P., Sinisterra, J., Leung, M. K., Shipp, M. A., Scharrer, B., and Stefano, G. B. (1990). Interaction of immunoactive monokines (IL-1 and TNF) in the bivalve mollusc Mytilus edulis.Proc. Natl. Acad. Sci. USA 874426–4429.

    Google Scholar 

  • Hughes, T. K., Smith, E. M., and Stefano, G. B. (1991). Detection of immunoreactive interleukin-6 in invertebrate hemolymph and nervous tissue.Prog. NeuroImmuneEndocrin. 4234–239.

    Google Scholar 

  • Kopec, S. (1917). Experiments on metamorphosis of insects.Bull. Acad. Polonaise Sci. Ser Sci. Math. Astron. Phys. 191757–60.

    Google Scholar 

  • Kopec, S. (1922). Studies on the necessity of the brain for the inception of insect metamorphasis.Biol. Bull. Woods Hole Mass. 42323–342.

    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 molluscMytilus edulis: Positive homotropic cooperativity of lower affinity binding sites.J. Biol. Chem., 2259218–9224.

    Google Scholar 

  • Leung, M., and Stefano, G. B. (1984). Isolation and identification of enkephalin in pedal ganglia ofMytilus edulis (mollusca).Proc. Natl. Acad. Sci. USA 81955–958.

    Google Scholar 

  • Leung, M. K., and Stefano, G. B. (1987). Comparative neurobiology of opioids in invertebrates with special attention to senescent alterations.Proq. Neurobiol. 28131–159.

    Google Scholar 

  • Leung, M. K., Le. S., Houston, S., and Stefano, G. B. (1992). Degradation of Met-enkephalin by hemolymph peptidases in Mytilus edulis.Cell. Mol. Neurobiol. (in press).

  • Lolait, S. J., Lim, A. T. W., Toh, B. H., and Fimder, J. W. (1984). Immunoreactive beta-endorphin in a subpopulation of mouse spleen macrophages.J. Clin. Invest. 73277–280.

    Google Scholar 

  • Lolait, S. J., Clements, J. A., Marwick, A. J., Cheng, C., McNally, M., Smith, A. I., and Funder, J. W. (1986). Proopiomelanocortin messenger ribonucleic acid and posttranslational processing of beta-endorphin in spleen macrophases.J. Clin. Invest. 771776–1781.

    Google Scholar 

  • Luschen, W., Buck, F., Willig, A., and Jaros, P. P. (1991). Isolation, sequence analysis, and physiological properties of enkephalins in the nervous tissue of the shore crabCarcinus maenas L.Proc. Natl. Acad. Sci. USA 888671–8675.

    Google Scholar 

  • Miller, G. C., Murgo, A. J., and Plotnikoff, N. P., (1983). Enkephalins enhancement of active T-cell rosettes from lymphoma patients.Clin. Immunol. Immunopathol. 26446–451.

    Google Scholar 

  • Miller, G. C., Murgo, A. J., and Plotnikoff, N. P., (1984). Enkephalins-enhancement of active T-cell rosettes from normal volunteers.Clin. Immunol. Immunopathol. 31132–136.

    Google Scholar 

  • Monstein, H.-J., Folkesson, R., and Terenius, L. (1986). Proenkephalin A-like mRNA in human leukemia leukocytes and CNS-tissues.Life Sci. 392237–2242.

    Google Scholar 

  • Ottaviani, E., Petraglia, F., Montagnan, G., Cossarizza, A. and Monti, D. (1990). Presence of ACTH andβ-endorphin immunoreactive molecules in the freshwater snailPlanorbarius corneus (L.) (Gastropoda, Pulmonata) and their possible role in phagocytosis.Regulat. Peptides 271–9.

    Google Scholar 

  • Prendergast, R. A., Lutty, G. A., and Scott, A. L. (1983). Directed inflammation: The phylogeny of lymphokines.Dev. Comp. Immunol. 7629–632.

    Google Scholar 

  • Ratcliffe, N. A. (1985). Invertebrate immunity—A primer for the non-specialist.Immunol. Lett. 10253–270.

    Google Scholar 

  • Renwrantz, L. (1990). Internal defense system of Mytilus edulis. InNeurobiology of Mytilus edulis (G. B. Stefano, Ed.), University of Manchester Press, Manchester, England, pp. 256–275.

    Google Scholar 

  • Renwrantz, L., and Stahmer, A. (1983). Opsonizing properties of an isolated hemolymph agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilus edulis.J. Comp. Physiol. 149535–546.

    Google Scholar 

  • Sawada, M., Hara, N., and Maeno, T., (1992). The reduction of the ACH-induced K+ current identified Aplysia neurons by human interleukin-1 and interleukin-2.Cell. Mol. Neurobiol. (in press).

  • Scharrer, B. (1978). Peptidergic neurons: Facts and trends.Gen. Comp. Endocrinol. 3450–62.

    Google Scholar 

  • Scharrer, B. (1987). Insects as models in neuroendocrine research.Ann. Rev. Entomol. 321–16.

    Google Scholar 

  • Shipp, M. A., Stefano, G. B., D'Adamio, L., Switzer, S. N., Howard, F. D., Sinisterra, J., Scharrer, B., and Reinherz, E. (1990). CD10/neutral endopeptidase 24.11 (“enkephalinase”) down regulates enkephalin-mediated inflammatory responses in invertebrate and mammalian organisms.Nature 347394–396.

    Google Scholar 

  • Shipp, M. A., Stefano, G. B., Switzer, S. N., Griffin, J. D., and Reinherz, E. L. (1991). CD10 (CALLA)/neutral endopeptidase 24.11 modulates inflammatory peptide-induced changes in neutrophil morphology, migration, and adhesion proteins and is itself regulated by neutrophil activation.Blood 781834–1841.

    Google Scholar 

  • Simon, E. J., Killer, 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 

  • Smith, E. M., Morrill, A. C., Meyer, W. J., III, and Blalock, J. E. (1986). Corticotropin releasing factor induction of leukocyte derived immunoreactive ACTH and endorphins.Nature 321881–883.

    Google Scholar 

  • Smith, E. M., Hughes, T. K., Scharrer, B., Leung, M. K., and Stefano, G. B. (1990). The production and action of ACTH related peptides in invertebrate hemocytes. Neuroimmunomodulation Congress, Florence, Italy, abstr. 3.4.

    Google Scholar 

  • Smith, E. M., Hughes, T. K., Leung, M. K., and Stefano, G. B. (1991). The production and action of ACTH-related peptides in invertebrate hemocytes.Adv. Neuroimmunol. 17–16.

    Google Scholar 

  • Smith, E. M., Hughes, T. K., Hashemi, F., and Stefano, G. B. (1992a). Immunosuppressive effects of ACTH and MSH and their possible significance in human immunodeficiency virus infection.Proc. Natl. Acad. Sci. USA 89782–786.

    Google Scholar 

  • Smith, E. M., Hughes, T. K., Cadet, P., and Stefano, G. B. (1992b). CRF induced immunosuppression in human and invertebrate immunocytesCell. Mol. Neurobiol. (in press).

  • Stefano, G. B. (1982). Comparative aspects of opioid-dopamine interaction.Cell. Mol. Neurobiol. 2167–178.

    Google Scholar 

  • Stefano, G. B. (1986). Conformational matching: A determining force in maintaining signal molecules. InComp. Opioid Relat. Neuropeptides Mech. (G. B. Stefano, Ed.), CRC Press, Boca Raton, FL, Vol. 2, pp. 271–277.

    Google Scholar 

  • Stefano, G. B. (1988). The evolvement of signal systems: Conformational matching a determining force stabilizing families of signal molecules.Comp. Biochem. Physiol. 90C287–294.

    Google Scholar 

  • Stefano, G. B. (1989). Role of opioid neuropeptides in immunoregulation.Prog. Neurobiol. 33149–159.

    Google Scholar 

  • Stefano, G. B. (1991). Conformational matching a stabilizing signal system factor during evolution: Additional evidence in comparative neuroimmunology.Adv. Neuroimmunol. 171–82.

    Google Scholar 

  • Stefano, G. B., and Leung, M. K., (1984). Presence of met-enkephalin-Arg-Phe in molluscan neural tissues.Brain Res. 298362–365.

    Google Scholar 

  • Stefano, G. B., and Martin, R. (1983). Enkephalin-like immunoreactivity in the pedal ganglion of Mytilus edulis (bivalvia) and its proximity to dopamine containing structures.Cell Tissue Res. 230147–153.

    Google Scholar 

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

    Google Scholar 

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

    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 Mytilus edulis (Bivalvia).J. Pharmacol. Exp. Ther. 222759–764.

    Google Scholar 

  • Stefano, G. B., Leung, M. K., Zhao, X., and Scharrer, B. (1989a). Evidence for the involvement of opioid neuropeptides in the adherence and migration of immunocompetent invertebrate hemocytes.Proc. Natl. Acad. Sci. USA 86626–630.

    Google Scholar 

  • Stefano, G. B., Cadet, P., and Scharrer, B. (1989b). Stimulatory effects of opioid neuropeptides on locomotory activity and conformational changes in invertebrate and human immunocytes: Evidence for a subtype of delta receptor.Proc. Natl. Acad. Sci. USA 866307–6311.

    Google Scholar 

  • Stefano, G. B., Zhao, X., Bailey, D., Metlay, M., and Leung, M. K. (1989c). High affinity dopamine binding to mouse thymocytes andMytilus edulis (Bivalvia) hemocytes.J. Neuroimmunol. 2167–74.

    Google Scholar 

  • Stefano, G. B., Shipp, M. A., and Scharrer, B. (1991a). A possible immunoregulatory function for Met.-enkephalin-Arg6-Phe7 involving human and invertebrate granulocytes.J. Neuroimmunol. 3197–103.

    Google Scholar 

  • Stefano, G. B., Smith, E. R., and Hughes, T. K. (1991b). Opioid induction of immunoreactive interleukin-1 inMytilus edulis and human immunocytes: An interleukin-1-like substance in invertebrate neural tissue.J. Neuroimmunol. 3229–34.

    Google Scholar 

  • Stefano, G. B., Cadet, P., Dokun A., and Scharrer, B. (1991c). A neuroimmunoregulatory-like mechanism responding to electrical shock in the marine bivalveMytilus edulis.Brain Behav. Immun. 4323–329.

    Google Scholar 

  • Stefano, G. B., Smith, D. M., Smith, E. M., and Hughes, T. K. (1991d). MSH can deactivate both TNF stimulated and spontaneously active immunocytes. InMolluscan Neurobiology (K. S. Kits, H. H. Boer and J. Joosse, Eds.), North-Holland, Amsterdam, pp. 206–209.

  • Stefano, G. B., Paemen, L. R., and Hughes, T. K. (1992). Autoimmunoregulation: Differential modulation of CD10/Neutral endopeptidase 24.11 by tumor necrosis factor and neuropeptides.J. Neuroimmunol. in press.

  • Szûcs, A., Stefano, G.B., Hughes, T. K., and S.-Rózsa, K. (1992). Modulation of voltage-activated ion currents on identified neurons ofHelix pomatia L. by interleukin-1.Cell. Mol. Neurobiol. (in press).

  • Zakarian, S., and Smyth, D. G. (1982). B-Endorphin is processed differently in specific regions of rat pituitary and brain.Nature (London)296250–252.

    Google Scholar 

  • Zurawski, G., Benedik, M., Kamb, B. J., Abrams, J. S., Zurawski, S. M., and Lee, F. D. (1986). Activation of mouse T-helper cells induces abundant preproenkephalin mRNA synthesis.Science 232772–775.

    Google Scholar 

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  1. Multidisciplinary Center for the Study of Aging, State University of New York, College at Old Westbury, 11568-0210, Old Westbury, New York, USA

    George B. Stefano

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Stefano, G.B. Invertebrate and vertebrate neuroimmune and autoimmunoregulatory commonalties involving opioid peptides. Cell Mol Neurobiol 12, 357–366 (1992). https://doi.org/10.1007/BF00711538

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