Skip to main content
Log in

Expression and translation of the egg-laying neuropeptide hormone genes during post-embryonic development of the pond snail Lymnaea stagnalis

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The neuroendocrine caudodorsal cells of Lymnaea stagnalis express two homologous genes, each encoding a polypeptide precursor. The precursors give rise to “cocktails” of neuropeptides that regulate egg-laying. The expression and translation of both egg-laying hormone genes during post-embryonic development were investigated by in situ hybridization and by electron-microscopic immunocytochemistry. Gene-II-specific transcripts and translation products were not found in caudodorsal cells in animals with shell heights smaller than 10 mm, in contrast to gene-I products that were present even at 3-mm shell height. The onset of expression of gene II coincides with the onset of release of products from the caudodorsal cells into the blood. Large electron-dense granules were found in caudodorsal cells of snails of all developmental stages investigated. These granules form part of the Golgi sorting and packaging pathway. Their presence suggests that differential sorting and packaging is possible during post-embryonic development, like in adults. The relationship of the differential expression of the two genes to the development of the caudodorsal cell system and its targets is discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Brussaard AB, Schluter NCM, Ebberink RHM, Kits KS, Ter Maat A (1991) Discharge induction in molluscan peptidergic cells requires a specific set of four auto-excitatory neuropeptides. Neuroscience 39:478–491

    Google Scholar 

  • Dirks RW, Raap AK, Van Minnen J, Vreugdenhil E, Smit AB, Ploeg M van der (1989) Detection of mRNA molecules coding for neuropeptides of the pond snail Lymnaea stagnalis by radioactive and non-radioactive in situ hybridization: a model study for mRNA detection. J Histochem Cytochem 37:7–14

    Google Scholar 

  • Dogterom GE, Loenhout H van, Geraerts WPM (1983) Synchronous maturation of the female reproductive system and of the ovulation hormone producing system in Lymnaea stagnalis. Gen Comp Endocrinol 52:242–246

    Google Scholar 

  • Ebberink RHM, Loenhout H van, Geraerts WPM (1985) Purification and amino acid sequence of the ovulation hormone of Lymnaea stagnalis. Proc Natl Acad Sci USA 82:7767–7771

    Google Scholar 

  • Geraerts WPM, Cheeseman P, Ebberink RHM, Nuyt K, Hogenes TM (1983) Partial purification and characterization of the ovulation hormone of the freshwater pulmonate snail Lymnaea stagnalis. Gen Comp Endocrinol 51:471–476

    Google Scholar 

  • Geraerts WPM, Ter Maat A, Vreugdenhil E (1988) The peptidergic neuroendocrine control of egg-laying behaviour in Aplysia and Lymnaea. In: Laufer H, Downer RGH (eds) Endocrinology of selected invertebrate types. Liss, New York, pp 144–231

    Google Scholar 

  • Kits KS (1980) States of excitability in ovulation hormone producing cells of Lymnaea stagnalis in relation to the egg-laying cycle. J Neurobiol 11:397–410

    Google Scholar 

  • Li KW, Geraerts WPM, Joosse J (1992) Purification and chemical characterization of caudodorsal cell hormone-II from the egg-laying controlling caudodorsal cells of Lymnaea stagnalis. Peptides 13:215–220

    Google Scholar 

  • Roubos EW (1976) Neuronal and non-neuronal control of the neurosecretory cells of the freshwater snail Lymnaea stagnalis (L.). Cell Tissue Res 168:11–31

    Google Scholar 

  • Roubos EW (1984) Cytobiology of the ovulation-hormone producing caudodorsal cells of the snail Lymnaea stagnalis. Int Rev Cytol 89:11–31

    Google Scholar 

  • Roubos EW, Winkoop A van, Haar C van der, Van Minnen J (1988) Postembryonic development of the endocrine dorsal bodies and neuroendocrine egg laying and growth hormone producing neurones of Lymnaea stagnalis. Int J Invert Reprod Dev 13:119–145

    Google Scholar 

  • Schmidt ED, Roubos EW (1987) Morphological basis for nonsynaptic communication within the central nervous system by exocytotic release of secretory material from the egg-laying stimulating neuroendocrine caudodorsal cells of Lymnaea stagnalis. Neuroscience 20:247–257

    Google Scholar 

  • Schmidt ED, Veenstra E, Broers-Vendrig CM, Ven A van de, Roubos EW (1989) Developmental and comparative aspects of nonsynaptic release by the egg-laying controlling caudodorsal cells of basommatophoran snails. Gen Comp Endocrinol 75:17–28

    Google Scholar 

  • Slootstra, JW (1993) Hormone-receptor binding. Protein motifs and antisense peptides. Thesis Free University Press, Amsterdam

  • Van Duivenboden YA (1983) Transfer of semen accelerates the onset of egg-laying in female copulants of the hermaphrodite snail Lymnaea stagnalis. Int J Invert Reprod 6:249–257

    Google Scholar 

  • Van Duivenboden YA (1984) Sexual behaviour of the hermaphrodite freshwater snail Lymnaea stagnalis. Thesis. Free University, Amsterdam

  • Van Heumen WRA, Roubos EW (1991) Immuno-electron microscopy of sorting and release of neuropeptides by Lymnaea stagnalis. Cell Tissue Res 264:185–195

    Google Scholar 

  • Van Heumen WRA, Broers-Vendrig CM, Roubos EW (1992) Light and electron immunocytochemical localization of synthesis, storage and release sites of the neuropeptide calfluxin of the caudodorsal cells of Lymnaea stagnalis. Gen Comp Endocrinol 87:361–368

    Google Scholar 

  • Van Minnen J, Reichelt D (1980) Neuronal regulation of the activity of neurosecretory cells in the lateral lobes of the cerebral ganglia of the pond snail Lymnaea stagnalis, with particular reference to the canopy cell. Proc R Dutch Acad Sci [C] 83:15–24

    Google Scholar 

  • Van Minnen J, Haar C van der, Raap AK, Vreugdenhil E (1988) Localization of ovulation hormone-like neuropeptide in the central nervous system of the snail Lymnaea stagnalis by means of immunocytochemistry and in situ hybridization. Cell Tissue Res 251:477–484

    Google Scholar 

  • Van Minnen J, Dirks RW, Vreugdenhil E, Diepen J van (1989a) Expression of the egg-laying hormone genes in peripheral neurones and exocrine cells in the reproductive tract of the mollusc Lymnaea stagnalis. Neuroscience 33:35–46

    Google Scholar 

  • Van Minnen J, Smit AB, Joosse J (1989b) Central and peripheral expression of genes encoding for egg-laying inducing and insulin-related peptides in a snail. Arch Histol Cytol 52:241–252

    Google Scholar 

  • Vreugdenhil E (1988) The molecular basis of egg-laying behaviour in the freshwater snail Lymnaea stagnalis. Thesis. Free University Press, Amsterdam

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

De Lange, R.P.J., van Minnen, J. & Boer, H.H. Expression and translation of the egg-laying neuropeptide hormone genes during post-embryonic development of the pond snail Lymnaea stagnalis . Cell Tissue Res 275, 369–375 (1994). https://doi.org/10.1007/BF00319436

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00319436

Key words

Navigation