Summary
the occurrence of insulin-related substances in the central nervous system of pulmonates and Aplysia californica was investigated by means of immunocytochemistry and in situ hybridization. Previous experiments have shown that, in Lymnaea stagnalis, the growth hormone-producing neurons in the cerebral ganglia (the so-called light green cells) express at least 5 genes that are related to the vertebrate insulin genes, i.e., they encode prohormones that are composed of a B- and A-chain and a connecting C peptide. These insulin related molecules also have the amino acids essential for their tertiary structure (viz. cysteines) at identical positions to those of the vertebrate insulins. In the investigated basommatophoran and stylommatophoran snails and slugs, neurons reacted with an antiserum raised against the C peptide of one of the molluscan insulin-related peptides. These neurons can be considered to be, based on morphological and endocrinological criteria, homologous to the light green cells of L. stagnalis. In A. californica, all central ganglia contain immunoreactive neurons. The highest number (about 50) was observed in the abdominal ganglion. The present results indicate that insulin-related substances are generally occurring neuropeptides in the central nervous system of molluscs.
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References
Blundell TL, Humbel RE (1980) Hormone families: pancreatic hormones and homologous growth factors. Nature 287:781–787
Capano CP, Guiditta A, Castigli E, Kaplan BB (1987) Occurrence and sequence complexity of polyadenylated RNA in squid axoplasm. J Neurochem 49:698–704
Froesch ER, Zapf J (1985) Insulin-like growth factors and insulin: comparative aspects. Diabetologia 28:485–493
Froesch ER, Schmid C, Schwander J, Zapf J (1985) Actions of insulin-like growth factors. Annu Rev Physiol 47:443–467
Geraerts WPM (1976) Control of growth by the neurosecretory hormone of the light green cells in the freshwater snail Lymnaea stagnalis. Gen Comp Endocrinol 29:61–71
Girbau M, Gomez JA, Lesniak MA, Pablo F de (1987) Insulin and insulin-like growth factor I both stimulate metabolism, growth, and differentiation in the post-neurula chick embryo. Endocrinology 121:1477–1482
Joosse J (1988) The hormones of molluscs. In: Laufer H, Downer GH (eds) Invertebrate Endocrinology Vol. 3. Endocrinology of selected invertebrate types. Alan R. Liss, New York, pp 89–140
McAllister LB, Scheller RH, Kandel ER, Axel R (1983) In situ hybridization to study the origin and fate of identified neurons. Science 222:800–808
Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Muzoguchi A, Fujiwara Y, Suzuki A, Takahashi SY, Ishizaki H (1986) Amino acid sequence of a prothoracicotropic hormone of the silkworm, Bombyx mori. Proc Natl Acad Sci USA 83:5840–5843
Price DA, Greenberg MJ (1977) Purification and characterization of a cardioexcitatory neuropeptide from the central ganglia of a bivalve mollusc. Prep Biochem 7:261–281
Raap AK, Geelen JL, Meer JWM van der, Rijke FM van der, Boogaart P van den, Ploeg M van der (1988) Non-radioactive in situ hybridization for the detection of cytomegalovirus infections. Histochemistry 88:367–377
Rapallino MV, Cupella A, Giuditta A (1988) Axoplasmic RNA species synthesized in the isolated squid axon. Neurochem Res 13:625–631
Roubos EW, Van De Ven AMH (1987) Morphology of neurosecretory cells in basommatophoran snails homologous with egg-laying and growth hormone-producing cells of Lymnaea stagnalis. Gen Comp Endocrinol 67:7–23
Roubos EW, Geraerts WPM, Boerrigter GM, Van Kampen GPJ (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 Lymnaea stagnalis (L.). Gen Comp Endocrinol 40:446–454
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
Steiner DF, Chan SJ, Welsh JM, Kwok SCM (1985) Structure and evolution of the insulin gene. Annu Rev Genet 19:463–484
Van Minnen J, Sokolove PG (1981) Neurosecretory cells in the central nervous system of the giant garden slug Limax maximus. J Neurobiol 12:297–301
Van Minnen J, Reichelt D, Lodder JC (1979) An ultrastructural study of the neurosecretory canopy cell of the pond snail Lymnaea stagnalis, with the use of the horseradish peroxidase tracer technique. Cell Tissue Res 204:453–462
Van Minnen J, Van De Haar Ch, Raap AK, Vreugdenhil E (1988) Localization of an 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
Van Minnen J, Smit AB, Joosse J (1989) Central and peripheral expression of genes coding for egg-laying and insulin-related peptides in a snail. Arch Histol Cytol [Suppl] 52:241–252
Vreugdenhil E, Jackson JF, Bouwmeester T, Smith AB, Van Minnen J, Van Heerikhuizen H, Klootwijk J, Joosse J (1988) Isolation, characterization and evolutionary aspects of a cDNA clone encoding multiple neuropeptides involved in a stereotyped egg-laying behaviour of the freshwater snail Lymnaea stagnalis. J Neurosci 81:4184–4191
Wendelaar Bonga SE (1970) Ultrastructure and histochemistry of neurosecretory cells and neurohaemal areas in the pond snail Lymnaea stagnalis. Z Zellforsch 108:190–224
Wijdenes J, Runham NW (1977) Studies on the control of growth in Agriolimax reticulatus (Mollusca, Pulmonata). Gen Comp Endocrinol 31:154–156
Wijdenes J, Van Minnen J, Boer HH (1980) A comparative study on neurosecretion demonstrated by the Alcian blue-Alcian yellow technique in three terrestrial pulmonates (Stylommatophora). Cell Tissue Res 210:47–56
Wijdenes J, Schlüter NCM, Gomot L, Boer HH (1987) In the snail Helix aspersa the gonadotropic hormone-producing dorsal bodies are under inhibitory nervous control of putative growth hormone-producing neuroendocrine cells. Gen Comp Endocrinol 68:224–229
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Van Minnen, J., Schallig, H.D.F.H. Demonstration of insulin-related substances in the central nervous systems of pulmonates and Aplysia californica . Cell Tissue Res 260, 381–386 (1990). https://doi.org/10.1007/BF00318640
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DOI: https://doi.org/10.1007/BF00318640