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Distribution and functional significance of Met-enkephalin-Arg6-Phe7-and Met-enkephalin-Arg6-Gly7-Leu8-like peptides in the blowflyCalliphora vomitoria

II. Immunocytochemical mapping of neuronal pathways in the retrocerebral complex and thoracic ganglion

Cell and Tissue Research volume 259, pages 147–157 (1990)Cite this article

Summary

Neuronal pathways in the retrocerebral complex and thoracico-abdominal ganglionic mass of the blowflyCalliphora vomitoria have been identified immunocytochemically with antisera against the extended-enkephalins, Met-enkephalin-Arg6-Phe7 (Met-7) and Met-enkephalin-Arg6-Gly7-Leu8 (Met-8). Neurons of the hypocerebral ganglion, immunoreactive to Met-8, have axons in the crop duct nerve and terminals in muscles of the crop and its duct. Certain neurons of the hypocerebral ganglion are also immunoreactive to Met-7, and axons from these cells innervate the heart. Met-8 immunoreactive nerve terminals invest the cells of the corpus allatum. The source of this material is believed to ve a single pair of lateral neurosecretory cells in the brain. There is no Met-7 immunoreactive material in the corpus allatum. In the corpus cardiacum neither Met-7 nor Met-8 immunoreactivity is present in the cells. However, in the neuropil of the gland certain fibres, with their origins elsewhere, do contain Met-8 immunoreactivity. The most prominent neurons in the thoracic ganglion are the Met-7 immunoreactive ventral thoracic neurosecretory cells, axons from which project to neurohaemal areas in the dorsal neural sheath and also, via the ventral connective, to the brain. Co-localisation studies show that the perikarya of these cells are immunoreactive to antisera raised against several vertebrate-type peptides, such as Met-7, gastrin/cholecystokinin and pancreatic polypeptide. However, their axons and terminals show varying amounts of the peptides, suggesting differential transport and utilisation. Only a few cells in the thoracic ganglion are immunoreactive to Met-8 antisera. These lie close to the nerve bundles suppling the legs. In the abdominal ganglion, Met-8 immunoreactive neurons project to the muscles of the hindgut. This study suggests that the extended enkephalin-like peptides ofCalliphora may have a variety of different roles: as neurotransmitter or neuromodulator substances; in the direct innervation of effector organs; and as neurohormones.

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References

  • Berridge MJ (1970) The role of 5-hydroxytryptamine and cyclic AMP in the control of fluid secretion by isolated salivary glands. J Exp Biol 53:171–186

    Google Scholar 

  • Berridge MJ, Patel NG (1968) Insect salivary glands: stimulation of fluid secretion by 5-hydroxytryptamine and adenosine-3, 5-monophosphate. Science 162:462–463

    Google Scholar 

  • Cook BJ, Holman GM (1980) Activation of potassium depolarised visceral muscles by protolin and caffeine in the cockroachLeucophaea maderae. Comp Biochem Physiol 67C:115–120

    Google Scholar 

  • Dalton T (1977) Threshold and receptor reserve in the action of 5-hydroxytryptamine on the salivary glandsCalliphora erythrocephala. J Insect Physiol 23:625–631

    Google Scholar 

  • Duve H, Thorpe A (1982) The distribution of pancreatic polypeptide in the nervous system and gut of the blowfly,Calliphora vomitoria (Diptera). Cell Tissue Res 237:415–426

    Google Scholar 

  • Duve H, Thorpe A (1984) Immunocytochemical mapping of gastrin/CCK-like peptides in the neuroendocrine system of the blowflyCalliphora vomitoria (Diptera). Cell Tissue Res 237:309–320

    Google Scholar 

  • Duve H, Thorpe A (1988) Mapping of enkephalin-related peptides in the nervous system of the blowfly,Calliphora vomitoria, and their co-localisation with cholecystokinin (CCK)-and pancreatic polypeptide (PP)-like peptides. Cell Tissue Res 251:399–415

    Google Scholar 

  • Duve H, Thorpe A (1989) Distribution and functional significance of Met-enkephalin-Arg6-Phe7-and Met-enkephalin-Arg6-Gly7-Leu8-like peptides in the blowfly,Calliphora vomitoria. I. Immunocytochemical mapping of neuronal pathways in the brain. Cell Tissue Res 258:147–161

    Google Scholar 

  • Duve H, Thorpe A, Nässel DR (1988) Light- and electron-microscopic immunocytochemistry of peptidergic neurons innervating thoracico-abdominal neurohaemal areas in the blowfly. Cell Tissue Res 253:583–595

    Google Scholar 

  • Ferri G-L, Morreale RA, Dockray GJ (1986) Met-enkephalin-Arg6-Gly7-Leu8 immunoreactivity in the human gut. Peptides 7:735–739

    Google Scholar 

  • Gupta BL, Berridge MJ (1966) Fine structural organization of the rectum in the blowfly,Calliphora erythrocephala (Meig) with special reference to connective tissue, trachaea and neurosecretory innervation in the rectal papilla. J Morphol 120:23–82

    Google Scholar 

  • Horikawa S, Takai T, Toyosato M, Takahashi H, Noda M, Kakidani H, Kubo T, Hirose T, Inayama S, Hayashida H, Miyata T, Numa S (1983) Isolation and structural organization of the human preproenkephalin B gene. Nature 306:611–614

    Google Scholar 

  • Kobayashi S, Suzuki M, Yanaihara N (1985) Enkephalin neurons in the guinea pig proximal colon: An immunocytochemical study using an antiserum to methionine-enkephalin-Arg6-Gly7-Leu8. Arch Histol Jpn 48:27–44

    Google Scholar 

  • Lea AO, Thomsen E (1969) Size independent secretion by the corpus allatum ofCalliphora erythrocephala. J Insect Physiol 15:477–482

    Google Scholar 

  • Mizoguchi A, Ishizaki H, Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Fujino M, Kitada C (1987) A monoclonal antibody against a synthetic fragment of bombyxin (4K-prothoracicotropic hormone) from the silkmoth,Bombyx mori: characterization and immunocytochemistry. Mol Cell Endocrinol 51:227–235

    Google Scholar 

  • Nachman RJ, Holman GM, Haddon WF, Ling N (1986) Leucosulfakinin, a sulphated insect neuropeptide with homology to gastrin and cholecystokinin. Science 234:71–73

    Google Scholar 

  • Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Mizoguchi A, Fujiwara Y, Suzuki A, Takahashi SY, Ishizaki H (1986) Amino acid sequence of a prothoracicotropic hormone of the silkwormBombyx mori. Proc Natl Acad Sci USA 83:5840–5843

    Google Scholar 

  • Nässel DR, Elekes K (1985) Serotonergic terminals in the neural sheath of the blowfly nervous system: ultrastructural immunocytochemistry and 5,7-dihydroxytryptamine labelling. Neuroscience 15:293–307

    Google Scholar 

  • Nichols R, Schnewly SA, Dixon JE (1988) Identification and characterization of aDrosophila homologue to the vertebrate neuropeptide cholecystokinin. J Biol Chem 263:12167–12170

    Google Scholar 

  • Normann TC (1965) The neurosecretory system of the adultCalliphora erythrocephala. I. The fine structure of the corpus cardiacum with some observations on adjacent organs. Z Zellforsch 67:461–501

    Google Scholar 

  • Normann TC (1972) Heart activity and its control in the adult blowfly,Calliphora erythrocephala. J Insect Physiol 18:1793–1810

    Google Scholar 

  • Sander GE, Giles TD (1985) Cardiovascular activities of intravenous methionine-enkephalin-Arg6-Phe7 and methionine-enkephalin-Arg6-Gly7-Leu8 in the conscious dog. Life Sci 36:2201–2207

    Google Scholar 

  • Shimosegawa T, Koizumi M, Toyota T, Goto Y, Mochizuki T, Yanaihara C, Yanhaihara N (1985) Met-enkephalin-Arg-Gly-Leu-like immunoreactivity-containing nerve elements in the guinea-pig intestine: an immunohistochemical study using whole mount preparations. Folia Endocrinol 61:802–815

    Google Scholar 

  • Smit AB, Vreugdenhil E, Ebberink RHM, Geraerts WPM, Klootwijk J, Joosse J (1988) Growth-controlling molluscan neurons produce the precursor of an insulin-related peptide. Nature 331:535–538

    Google Scholar 

  • Stefano GB (1986) Handbook of comparative opioid and related neuropeptide mechanisms. CRC Press Inc. Boca Raton, Florida

    Google Scholar 

  • Thomsen E (1940) Relation between corpus allatum and ovaries in adult flies (Muscidae). Nature 145:28

    Google Scholar 

  • Thomsen E (1954) Studies on the transport of neurosecretory material by means of ligaturing experiments. J Exp Biol 31:322–330

    Google Scholar 

  • Thomsen M (1969) The neurosecretory system of the adultCalliphora erythrocephala. IV. A histological study of the corpus cardiacum and its connections to the nervous system. Z Zellforsch 94:205–219

    Google Scholar 

  • Thomsen E, Thomsen M (1970) Fine structure of the corpus allatum of the female blowflyCalliphora erythrocephala. Z Zellforsch 110:40–60

    Google Scholar 

  • Tobe SS, Stay B (1985) Structure and regulation of the corpus allatum. Adv Insect Physiol 18:305–432

    Google Scholar 

  • Wasserthal LT, Wasserthal W (1977) Innervation of heart and alary muscles inSphinx ligustri L. Lepidoptera. Cell Tissue Res 184:467–486

    Google Scholar 

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  1. School of Biological Sciences, Queen Mary College, London University, London, United Kingdom

    Hanne Duve & Alan Thorpe

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  1. Hanne Duve
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  2. Alan Thorpe
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Duve, H., Thorpe, A. Distribution and functional significance of Met-enkephalin-Arg6-Phe7-and Met-enkephalin-Arg6-Gly7-Leu8-like peptides in the blowflyCalliphora vomitoria . Cell Tissue Res. 259, 147–157 (1990). https://doi.org/10.1007/BF00571439

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Key words

  • Immunocytochemistry
  • Met-enkephalin-Arg6-Phe7
  • Met-enkephalin-Arg6-Gly7-Leu8
  • Neurosecretory cells of insects
  • Neuropeptides
  • Co-existence of peptides
  • Blowfly,Calliphora vomitoria (Insecta)