Cellular and Molecular Neurobiology

, Volume 8, Issue 3, pp 269–284 | Cite as

Opioid mechanisms in insects, with special attention toLeucophaea maderae

  • Berta Scharrer
  • George B. Stefano
  • Michael K. Leung


  1. 1.

    This review article provides information on the evolutionary history of neuroendocrine and related regulatory mechanisms. It focuses on the presence, diverse roles, and modes of operation of one class of neuropeptides, the endogenous opioids, in insects.

  2. 2.

    Opioid peptides, closely resembling those of vertebrates, have been identified in the brain and related neuroendocrine structures by means of immunocytochemistry and high-pressure liquid chromatography.

  3. 3.

    The demonstration of naloxone-sensitive, high-affinity binding sites for Met-enkephalin-like neuropeptides in the brain and digestive tract ofLeucophaea deserves special attention because it provides new insights into the functional significance of opiate receptors paralleling those known in vertebrates.

  4. 4.

    Possible roles of receptor-mediated opioid systems in the insects discussed are regulation of the cyclicity of the female reproductive system, maintenance of normal midgut function mediated by the recurrent nerve, and locomotor activity.


Key words

neuroendocrine mechanisms evolutionary history neuropeptides endogenous opioids immunocytochemistry HPLC opioid receptors 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andriès, J. C., and Tramu, G. (1985). Ultrastructural and immunohistochemical study of endocine cells in the midgut of the cockroachBlaberus craniifer (Insecta, Dictyoptera).Cell Tissue Res. 240323–332.Google Scholar
  2. Audigier, Y., Duprat, A. M., and Cros, J. (1980). Comparative study of opiate and enkephalin receptors on lower vertebrates and higher vertebrates.Comp. Biochem. Physiol. 67191–193.Google Scholar
  3. Chapman, A., Gonzales, G., Burrowes, W. R., Assanah, P., Iannone, B., Leung, M. K., and Stefano, G. B. (1984). Alterations in high affinity binding characteristics and levels of opioids in invertebrate ganglia during aging: Evidence for an opioid compensatory mechanism.Cell. Mol. Neurobiol. 4143–155.Google Scholar
  4. Committee on Models for Biomedical Research (1985).Models for Biomedical Research: A New Perspective, Natl. Acad. Sci. Press, Washington, D.C.Google Scholar
  5. Duve, H., and Thorpe, A. (1984). Immunocytochemical mapping of gastrin/CCK-like peptides in the neuroendocrine system of the blowfly,Calliphora vomitoria (Diptera).Cell Tissue Res. 237309–320.Google Scholar
  6. Duve, H., Thorpe A., and Scott, A. (1986). Localization and characterization of opioid-like peptides in the nervous system of the blowfly,Calliphora vomitoria. InHandbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol. 1 (Stefano, G. B., Ed.), CRC Press, Boca Raton, Fla., pp. 197–211.Google Scholar
  7. El-Salhy, M., Falkmer, S., Kramer, K. J., and Speirs, R. D. (1983). Immunohistochemical investigations of neuropeptides in the brain, corpora cardiaca, and corpora allata of an adult lepidopteran insect,Manduca sexta.Cell Tissue Res. 232295–317.Google Scholar
  8. Ford, R., Jackson, D. M., Tetrault, L., Torres, J. C., Assanah, P., Harper, J., Leung, M. K., and Stefano, G. B. (1986). A behavioral role for enkephalins in regulating locomotor activity in the insectLeucophaea maderae: Evidence for high affinity kappa-like opioid binding sites.Comp. Biochem. Physiol. 85C61–66.Google Scholar
  9. Gersch, M., and Richter, K. (eds.) (1981).Das Peptiderge Neuron, Gustav Fischer Verlag, Jena.Google Scholar
  10. Greese, I., and Snyder, S. H. (1975). Receptor binding and pharmacological activity of opiates in the guinea-pig intestine.J. Pharmacol. Exp. Ther. 194205–219.Google Scholar
  11. Hansen, B. L., Hansen, G. N., and Scharrer, B. (1982). Immunoreactive material resembling vertebrate neuropeptides in the corpus cardiacum and corpus allatum of the insectLeucophaea maderae.Cell Tissue Res. 225319–329.Google Scholar
  12. Hansen, B. L., Hansen, G. N., and Scharrer, B. (1986). Immunocytochemical demonstration of a material resembling vertebrate ACTH and MSH in the corpus cardiacum-corpus allatum complex of the insectLeucophaea maderae. InHandbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol. 1, (Stefano, G. B., Ed.), CRC Press, Boca Raton, Fla., pp. 213–222.Google Scholar
  13. Hansen, G. N., Hansen, B. L., and Scharrer, B. (1987). Gastrin/CCK-like immunoreactivity in the corpus cardiacum-corpus allatum complex of the cockroachLeucophaea maderae.Cell Tissue Res. 248595–598.Google Scholar
  14. Hiller, J. M., Simon, E. J., Crain, S. M., and Peterson, E. R. (1978). Opiate receptors in cultures of fetal mouse dorsal root ganglia (DRG) and spinal cord: Predominance in DRG neurites.Brain Res. 245396–400.Google Scholar
  15. Iwanga, T., Fujita, T., Nishiitsutsuji-Uwo, J., and Endo, Y. (1981). Immunohistochemical demonstration of PP-, somatostatin-, enteroglucagon- and VIP-like immunoreactivities in the cockroach midgut.Biomed. Res. 2202–207.Google Scholar
  16. Jaros, P. P., Dircksen, H., and Keller, R. (1985). Occurrence of immunoreactive enkephalins in a neurohemal organ and other nervous structures in the eyestalk of the shore crab,Carcinus maenas L. (Crustacea, Decapoda).Cell Tissue Res. 241111–117.Google Scholar
  17. Jessell, T. M., and Iversen, L. L. (1977). Opiate analgesics inhibit substance P release from rat trigeminal nucleus.Nature (Lond.)268549–551.Google Scholar
  18. Kavaliers, M., and Hirst, M. (1987). Slugs and snails and opiate tales: Opioids and feeding behavior in invertebrates.Fed. Proc. 46168–172.Google Scholar
  19. Kavaliers, M., Hirst, M., and Teskey, G. C. (1983). A functional role for an opiate system in snail thermal behavior.Science 22099–101.Google Scholar
  20. Kopeć, S. (1917). Experiments on metamorphosis of insects.Bull. Acad. Sci. Cracovie Sci. Math. Nat. Ser. B 191757–60.Google Scholar
  21. Kopeć, S. (1922). Studies on the necessity of the brain for the inception of insect metamorphosis.Biol. Bull. Woods Hole Mass. 42323–342.Google Scholar
  22. 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. 2259218–9224.Google Scholar
  23. Lamotte, C., Pert, C. D., and Snyder, S. H. (1976). Opiate receptor binding in primate spinal cord: Distribution and changes after dorsal root section.Brain Res. 112407–412.Google Scholar
  24. Leung, M. K., and Stefano, G. B. (1984). Isolation and identification of enkephalins in pedal ganglia ofMytilus edulis (Mollusca).Proc. Natl Acad. Sci. USA 81955–958.Google Scholar
  25. Leung, M. K., and Stefano, G. B. (1987). Comparative neurobiology of opioids in invertebrates with special attention to senescent alterations.Progr. Neurobiol. 28131–159.Google Scholar
  26. Pert, C. D., and Snyder, S. H. (1974). Opiate receptor binding of agonists and antagonists affected differentially by sodium.Mol. Pharmacol. 10808–879.Google Scholar
  27. Pert, C. D., and Taylor, D. (1980). Type 1 and type 2 opiate receptors: A subclassification scheme based upon GTP's differential effects on binding. InEndogenous and Exogenous Opiate Agonists and Antagonists (Way, E. L., Ed.), Pergamon Press, New York, pp. 87–94.Google Scholar
  28. Pollard, H., Llorens-Cortes, C., and Schwartz, J. C. (1977). Enkephalin receptors in dopaminergic neurons in rat striatum.Nature (Lond.)268745–747.Google Scholar
  29. Pollard, H., Llorens, C., Schwartz, J. C., Gros, C., and Dray, F. (1987). 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
  30. Rémy, C., and Dubois, M. P. (1981). Immunohistological evidence of methionine enkephalin-like material in the brain of the migratory locust.Cell Tissue Res. 218271–278.Google Scholar
  31. Rémy, C. H., Girardie, J., and Dubois, M. P. (1978). Présence dans le ganglion sous-oesophagien de la Chenille processionaire du Pin (Thaumetopoea pityocampa Schiff) de cellules revelées en immunofluorescence par un anticorps anti-alpha-endorphine.C.R. Acad. Sci. Paris Sér. D. 286651–653.Google Scholar
  32. Santoro, C., Hall, L. H., and Zukin, R. S. (1985). Opioid receptor subtypes inDrosophila melanogaster. Int. Narcotic Res. Conf., Falmouth, Mass., Abstr. 0-22.Google Scholar
  33. Scharrer, B. (1945). Experimental tumors after nerve section in an insect.Proc. Soc. Exp. Biol. Med. 60184–189.Google Scholar
  34. Scharrer, B. (1978). Peptidergic neurons: Facts and trends.Gen. Comp. Endocrinol. 3450–62.Google Scholar
  35. Scharrer, B. (1987a). Insects as models in neuroendocrine research.Ann. Rev. Entomol. 321–16.Google Scholar
  36. Scharrer, B. (1987b). Neurosecretion: Beginnings and new directions in neuropeptide research.Ann. Rev. Neurosci. 101–17.Google Scholar
  37. Schols, D., Verhaert, P., Huybrechts, R., Vaudry, H., Jégou, S., and De Loof, A. (1987). Immunocytochemial demonstration of proopiomelanocortin- and other opioid-related substances and a CRF-like peptide in the gut of the american cockroach,Periplaneta americana L.Histochemistry 86345–351.Google Scholar
  38. Schulz, R., Wuster, M., and Herz, A. (1979). Supersensitivity to opioids following the chronic blockade of endorphin action by naloxone.Naunyn-Schmiedeberg Arch. Pharmacol. 30693–96.Google Scholar
  39. Simon, E. J., Hiller, J. M., Groth, J., and Edelman, I. (1975). Further properties of stereospecific opiate binding in rat brain: On the nature of the sodium effect.J. Pharmacol. Exp. Ther. 192531–537.Google Scholar
  40. Stefano, G. B. (1982). Comparative aspects of opioid-dopamine interaction.Cell. Mol. Neurobiol. 2167–178.Google Scholar
  41. Stefano, G. B. (1986). Conformational matching: A determining force in maintaining signal molecules. InHandbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol. 2 (Stefano, G. B., Ed.), CRC Press, Boca Raton, Fla., pp. 271–277.Google Scholar
  42. Stefano, G. B., and Catapane, E. J. (1980). Norepinephrine: Its presence in the CNS of the bivalve mollusc,Mytilus edulis.J. Exp. Zool. 214209–213.Google Scholar
  43. Stefano, G. B., and Leung, M. K. (1984). Presence of met-enkephalin-arg-phe in molluscan neural tissues.Brain Res. 298362–365.Google Scholar
  44. Stefano, G. B., and Scharrer, B. (1981). High affinity binding of an enkephalin analog in the cerebral ganglion of the insectLeucophaea maderae (Blattaria).Brain Res. 225107–114.Google Scholar
  45. 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. 181440–445.Google Scholar
  46. 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
  47. Stefano, G. B., Scharrer, B., and Assanah, P. (1982). Demonstration, characterization and localization of opioid binding sites in the midgut of the insectLeucophaea maderae (Blattaria).Brain Res. 253205–212.Google Scholar
  48. Takeda, S., Vieillemaringe, J., Geffard, M., and Rémy, C. (1986). Immunohistological evidence of dopamine cells in the cephalic nervous system of the silkwormBombyx mori. Coexistence of dopamine and alpha-endorphin-like substance in neurosecretory cells of the suboesophageal ganglion.Cell Tissue Res. 243125–28.Google Scholar
  49. Veenstra, J. A., Romberg-Privee, H. M., Schooneveld, H., and Polak, J. M. (1985). Immunocytochemical localization of peptidergic neurons and neurosecretory cells in the neuroendocrine system of the Colorado potato beetle with antisera to vertebrate regulatory peptides.Histochemistry 829–18.Google Scholar
  50. Verhaert, P., and De Loof, A. (1985). Immunocytochemical localization of a methionine-enkephalin-resembling neuropeptide in the central nervous system of the American cockroach,Periplaneta americana L.J. Comp. Neurol. 23954–61.Google Scholar
  51. Waterfield, A. A., Smokcum, R. W. J., Hughes, J., Kosterlitz, H. W., and Henderson, G. (1977). In vitro pharmacology of the opioid peptides, enkephalins and endorphins.Eur. J. Pharmacol. 43107–116.Google Scholar
  52. Way, E. L. (Ed.) (1980).Endogenous and Exogenous Opiate Agonists and Antagonists, Pergamon Press, New York.Google Scholar
  53. Weiss, A., and Penzlin, H. (1987). Effect of morphine and naloxone on shock avoidance learning in headless cockroaches (Periplaneta americana L.).Physiol. Behav. 39445–451.Google Scholar

Copyright information

© Plenum Publishing Corporation 1988

Authors and Affiliations

  • Berta Scharrer
    • 1
  • George B. Stefano
    • 2
  • Michael K. Leung
    • 3
  1. 1.Department of Anatomy and Structural Biology and Department of NeuroscienceAlbert Einstein College of MedicineBronxUSA
  2. 2.Multidisciplinary Center for the Study of Aging and Biological Sciences ProgramSUNY/College at Old WestburyOld WestburyUSA
  3. 3.Multidisciplinary Center for the Study of Aging and Chemistry/Physics ProgramSUNY/College at Old WestburyOld WestburyUSA

Personalised recommendations