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Neurosecretion pp 123-135 | Cite as

Biosynthesis and Release of Multiple Peptides by the Caudodorsal Cells of Lymnaea Stagnalis

  • E. W. Roubos

Abstract

The peptidergic Caudodorsal Cells (CDC) of the freshwater snail Lvmnaea stagnalis control egg laying and egg-laying behaviour by releasing various peptides that act upon different targets (e.g., Roubos, 1984; Geraerts et al., 1987). Egg laying lasts about 2 hours and involves ovulation of up to 200 oocytes from the ovotestis, packaging of these cells by various types of female accessory sex gland into an egg mass, and oviposition. Overt egg-laying behaviour consists of a number of stereotyped behavioural acts (Goldschmeding et al., 1983). It begins with cessation of locomotion and posture changes. After about one hour the animal starts crawling about and cleans the substrate by rasping with its buccal mass before depositing the egg capsule. Actual oviposition takes 10–20 minutes depending on the size of the egg mass (Dogterom et al., 1983). Finally, the animal crawls back along the egg mass, touching it with the lip, before moving off. In this paper a brief survey will be given of the mechanisms by which CDC activity is controlled, of the way the CDC synthesize and release their peptides, and of the effects of the CDC peptides upon their targets. This may help to clarify how the CDC initiate an egg-laying behaviour that is coordinated with other important physiological processes such as feeding, locomotion and copulation (Fig. 1). Particular attention will be paid to structure-function relationships of the CDC-system.

Keywords

Secretory Granule Cerebral Ganglion Freshwater Snail Pond Snail Albumen Gland 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Buma, P., and Roubos, E.W., 1983, Calcium dynamics, exocytosis, and membrane turnover in the ovulation-hormone releasing caudo-dorsal cells of Lvmnaea stagnalis, Cell Tiss. Res., 233: 143.CrossRefGoogle Scholar
  2. Buma, P., Roubos, E.W., and Buijs, R.M., 1984, Ultrastructural demonstration of exocytosis of neural, neuroendocrine and endocrine secretions with an in vitro tannic acid ( TARI-) method, Histochemistrv, 80: 247.CrossRefGoogle Scholar
  3. Buma, P, and Roubos, E.W., 1986, Ultrastructural demonstration of nonsynaptic release sites in the brain of the snail Lvmnaea stagnalis, the insect Periolaneta americana, and the rat, Neuroscience, 17: 867.CrossRefGoogle Scholar
  4. Buma, P., Roubos, E.W., and Brunekreef, K., 1986, Role of cAMP in electrical and secretory activity of the neuroendocrine caudo-dorsal cells of Lymnaea stagnalis, Brain Res., 380: 26.CrossRefGoogle Scholar
  5. Chiu, A.Y., Hunkapillar, M.W., Heller, E., Stuart, D.K., Hood, L.E., and Strumwasser, F., 1979, Purification and primary structure of the neuropeptide egg-laying hormone of Anivsia californica, Proc. Natl. Acad. Sci. U.S.A., 76: 6656.CrossRefGoogle Scholar
  6. Dictus, W.J.A.G., Jong-Brink, M. de, and Boer, H.H., 1987, A neuropeptide (calfluxin) is involved in the influx of calcium into mitochondria of the albumen gland of the freshwater snail Lvmnaea stagnalis, Gen. Comn. Endocrinol., 65: 439.CrossRefGoogle Scholar
  7. Dogterom, G.E., Bohlken, S., and Joosse, J., 1983, Effect of the photoperiod on the time schedule of egg mass production in Lvmnaea stagnalis, as induced by ovulation hormone injections, Gen. Como. Endocrinol., 49: 255.CrossRefGoogle Scholar
  8. Dogterom, G.E., Thijssen, R., and Loenhout, H. van, 1985, Environmental and hormonal control of the seasonal egg-laying period in field specimens of Lvmnaea stagnalis, Gen. Comn. Endocrinol., 57: 37.CrossRefGoogle Scholar
  9. Ebberink, R.H.M., Loenhout, H. van, Geraerts, W.P.M., and Joosse, J. 1985, Purification and amino acid sequence of the ovulation neurohormone of Lvmnaea stagnalis, Proc. Natl. Acad. Sci. U.S.A., 82: 7767.CrossRefGoogle Scholar
  10. Geraerts, W.P.M., 1976, The role of the lateral lobes in the control of growth and reproduction in the hermaphrodite freshwater snail Lvmnaea stagnalis, Gen. Como. Endocrinol., 19: 97.CrossRefGoogle Scholar
  11. Geraerts, W.P.M., Maat, A. ter, and Hogenes, T.M., 1984, Studies on release activities of the neurosecretory caudo-dorsal cells of Lvmnaea stagnalis, pp 44–50, in: “Biosynthesis, Metabolism and Mode of Action of Invertebrate Hormones,” J. Joffmann, and M. Porchet, eds., Springer, Berlin.Google Scholar
  12. Geraerts, W.P.M., Vreugdenhil, E., Ebberink, R.H.M., and Hogenes, T.M., 1985, Synthesis of multiple peptides from a larger precursor in the neuroendocrine caudo-dorsal cells of Lvmnaea stagnalis, Neurosci. Lett., 56: 241.CrossRefGoogle Scholar
  13. Geraerts, W.P.M., Maat, A. ter, and Vreugdenhil, E., 1987, The peptidergic neuro-endocrine control of egg-laying behavior in Aolvsia and Lvnmaea, in: “Invertebrate Endocrinology,” Vol. 2, H. Laufer, and R. Downer, eds., Liss, New York, ( In Press ).Google Scholar
  14. Goldschmeding, J.T., Wilbrink, M., and Maat, A. ter, 1983, The role of the ovulation hormone in the control of egg-laying behaviour in Lvmnaea stagnalis, pp 251–255, in: Molluscan neuro-endocrinology, J. Lever, and H.H. Boer, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  15. Jansen, R.F., 1984, Neuronal and hormonal control of the egg-laying behavior in the pond snail Lvmnaea stagnalis, Thesis, Vrije Universiteit, Amsterdam.Google Scholar
  16. Jensen, R.F., and Maat, A. ter, 1985, Ring neuron control of columellar motor neurons during egg-laying behavior in the pond snail, J. Neurobiol., 16: 1.CrossRefGoogle Scholar
  17. Joosse, J., 1964, Dorsal bodies and dorsal neurosecretory cells of the cerebral ganglia of Lvmnaea stagnalis L., Arch. Neerl. de Zool., 15: 1.CrossRefGoogle Scholar
  18. Kits, K.S., 1980, States of excitability in ovulation hormone producing neuroendocrine cells of Lvmnaea stagnalis ( Gastropoda) and their relation to the egg-laying cycle, J. Neurobiol., 11: 397.CrossRefGoogle Scholar
  19. Maat, A. ter, Roubos, E.W., Lodder, J.C., and Buma, P., 1983, Integration of biphasic synaptic input by electrotonically coupled neuroendocrine caudo-dorsal cells in the pond snail, J. Neurophvsiol., 49: 1392.Google Scholar
  20. Maat, A. ter, Dijcks, F.A., and Bos, N.P.A., 1986, In vivo recordings of neuroendocrine cells (caudo-dorsal cells) in the pond snail, J. Comp. Phvsiol. A, 158: 853.CrossRefGoogle Scholar
  21. Mahon, A.C., Nambu, J.R., Taussig, R., Shyamala, M., Roach, A., and Scheller, R.H., 1985, Structure and expression of the egg-laying hormone gene family in Aplysia, J. Neurosci., 5: 1872.Google Scholar
  22. Minnen, J. van, and Vreugdenhil, E., 1987, The occurrence of gonadotropic hormones in the central nervous system and reproductive tract of Lvmnaea stagnalis. An immunocytochemical and in situ hybridization study, pp. 62–67, in: Neurobiology. Molluscan models, H.H. Boer, W.P.M. Geraerts, and J. Joosse, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  23. Minnen, J. van, Haar., C. van der, Raap, A.K., and Vreugdenhil, E., 1987, Localization of ovulation hormone-like neuropeptide in the central nervous system of the snail Lvmnaea stagnalis with immunocytochemistry and in situ hybridization, Cell Tiss. Res.Google Scholar
  24. Moed, P.J., Boss, N.P.A., Kits, K.S., Maat, A. ter, 1987, The role of release products and second messengers in the regulation of electrical activity of the neuroendocrine caudodorsal cells of Lvmnaea stagnalis, pp. 194–199, in Neurobiology. Molluscan models, H.H. Boer, W.P.M. Geraerts, and J. Joosse, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  25. Müller, L.J., Ven, A.H.M., van de, and Roubos, E.W., 1987, Neurons of the snail Lvmnaea stagnalis as a model for the study of clinical neurotoxic side effects of anti-tumor agents, pp. 138–142, in: Neurobiology, Molluscan models, H.H. Boer, W.P.M. Geraerts, and J. Joosse, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  26. Roubos, E.W., 1984, Cytobiology of the ovulation-neurohormone producing caudo-dorsal cells of the snail Lvmnaea stagnalis, Int. Rev. Cvtol., 89: 295.CrossRefGoogle Scholar
  27. Roubos, E.W., 1985, Intracellular and extracellular control of neuroendocrine activity in the freshwater snail Lvmnaea stagnalis, pp 47–49, in: Current trends in comparative endocrinology, B. Lofts, and W.N. Holmes, eds., Hong Kong.Google Scholar
  28. Roubos, E.W., and Wal-Divendal. R.M. van der, 1980, Ultrastructural analysis of peptide-hormone release by exocytosis, Cell Tiss. Res., 207: 267.CrossRefGoogle Scholar
  29. Roubos, E.W., and Ven, A.M.H. van de, 1987, Morphology of neurosecretory cells in Basommatophoran snails homologous with egg-laying and growth-hormone producing cells of Lvmnaea stagnalis, Gen. Comp. Endocrinol., (In press).Google Scholar
  30. Roubos, E.W., Geraerts, W.P.M., Boerrigter, G.H. and Kampen, G.P.J. van, 1980, Control of activities of the neurosecretory light green and caudodorsal cells and of the endocrine dorsal bodies by the lateral lobes in the freshwater snail Lvmnaea stagnalis (L.), Gen. Come. Endocrinol., 40: 446.CrossRefGoogle Scholar
  31. Roubos, E.W., Keijzer, A.N. de, and Buma, P., 1981a, Adenylate cyclase activity in axon terminals of ovulation-hormone producing neuroendocrine cells in Lvmnaea stagnalis Cell Tiss. Res., 220: 665.Google Scholar
  32. Roubos, E.W., Schmidt, E.D., and Moorer-van Delft, C.M., 1981b, Ultrastructural dynamics of exocytosis in the ovulation neurohormone producing caudo-dorsal cells of the freshwater snail Lvnmaea stagnalis ( L. ), Cell Tiss. Res., 215: 63.CrossRefGoogle Scholar
  33. Roubos, E.W., Buma, P., and Roos, W.F. de, 1983, Ultrastructural correlates of electronic and neurochemical communication in Lvmnaea stagnalis, with particular reference to nonsynaptic transmission and neuroendocrine cells, pp 78–81, in: Molluscan neuro-endocrinology. J. Lever, and H.H. Boer, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  34. Roubos, E.W., Leeuwen, J.P.T.M. van, and Maijers, A., 1985, Ultrastructure of gap junctions in the central nervous system of Lvmnaea stagnalis, with particular reference to electrotonic coupling between the neuroendocrine caudo-dorsal cells, Neuroscience, 14: 711.CrossRefGoogle Scholar
  35. Roubos, E.W., Ven, A.M.H. van de, and Minnen, J. van, 1987a, Immunoelectron microscopy of formation, degradation and exocytosis of the ovulation neurohormone of Lvmnaea stagnalis, Cell Tiss. Res., (In press).Google Scholar
  36. Roubos, E.W., Ven, A.M.H. van der, Schmidt, E.D., and Heumen, W.R.A. van, 1987b, Structural aspects of biosynthesis, storage and release of neuropeptides in freshwater snails, pp. 82–88, in: Neurobiology. Molluscan models, H.H. Boer, W.P.M. Geraerts, and J. Joosse, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  37. Schmidt, E.D., and Roubos, E.W., 1987a, Morphological basis for nonsynaptic communication within the central nervous system by exocytotic release of secretory material from the egg-laying stimulating neuroendocrine caudo-dorsal cells of Lvmnaea stagnalis, Neuroscience, 20: 247.CrossRefGoogle Scholar
  38. Schmidt, E.D., and Roubos, E.W., 1987b, Morphology and dynamics of nonsynaptic release sites of the caudo-dorsal cells of Lvmnaea stagnalis, pp. 89–94, in: Neurobiology. Molluscan models, H.H. Boer, W.P.M. Geraerts, and J. Joosse, eds., North-Holland Publishing Company, Amsterdam.Google Scholar
  39. Schmitt, F.O., 1984, Molecular regulators of brain function: a new view, Neuroscience, 13: 991.CrossRefGoogle Scholar
  40. Vlieger, T.A. de, Kits, K.S., Maat, A. ter, and Lodder, J.C., 1980, Morphology and electrophysiology of the ovulation hormone producing neuro-endocrine cells of the freshwater snail Lvmnaea stagnalis ( L. ), J. Exo. Biol., 84: 259.Google Scholar
  41. Vreugdenhil, E., Geraerts, W.P.M., Jackson, J.F., and Joosse, J., 1985, The molecular basis of the neuro-endocrine control of egg-laying behaviour in Lvmnaea, Pevtides, 6 (suppl. 3): 465.CrossRefGoogle Scholar
  42. Wendelaar Bonga, S.E., 1971, Formation, storage, and release of neurosecretory material studied by quantitative electron microscopy in the freshwater snail Lvmnaea staQnalis ( L.), Z. Zellforsch., 113: 490.Google Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • E. W. Roubos

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