Abstract
Embryogenesis of the histaminergic system in the pond snail, Lymnaea stagnalis, was investigated by means of immunocytochemistry and HPLC assay. From the earliest onset of the of histamine-immunoreactive (HA-IR) elements, the labelled neurons were confined to the pedal, cerebral and buccal ganglia, whereas no IR cells within the pleural, parietal and visceral ganglia were detectable during the embryogenesis. Peripheral projections of the embryonic HA-IR neurons were missing. No transient HA-IR neurons could be found either inside or outside the CNS. The first HA-IR elements appeared at about E55% of embryonic development, at the beginning of metamorphosis, and were represented by three pairs of neurons located in the cerebral ganglia. Following metamorphosis, four pairs of HA-IR neurons were added; two of them occurred in the pedal (E65% stage of development) and two in the buccal (E90% stage of development) ganglia. During embryogenesis, HA-IR fibers were present in the cerebro-pedal connectives and in the cerebral, pedal and buccal commissures, whereas only little arborization could be observed in the neuropil of the ganglia. HPLC measurements revealed a gradual increase of HA content in the embryos during development, corresponding well to the course of the appearance of immunolabeled elements. It is suggested that the developing HAergic system plays a specific role in the process of gangliogenesis and CNS plasticity of embryonic Lymnaea.
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Battelle, B. A., Calman, B. G., Andrews, A. W., Grieco, F. D., Mleziva, M. B., Callaway, J. C., Stuart, A. E. (1991) Histamine: a putative afferent neurotransmitter in Limulus eyes. J. Comp. Neurol. 305, 527–542.
Benjamin, P. R., Burke, J. F. (1994) Alternative mRNA splicing of the FMRFamide gene and its role in neuropeptidergic signalling in a defined neural network. BioEssays 16, 335–342.
Benjamin, P. R., Staras, K., Kemenes, G. (2000) A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learning and Memory 7, 124–131
Brown, R. E., Stevens, D. R., Haas, H. L. (2001) The physiology of brain histamine. Prog. Neurobiol. 63, 637–672.
Buchner, E., Buchner, S. M. G., Hofbauer, A., Pak, W. L., Pollack, I. (1993) Histamine is a major mechanosensory neurotransmitter candidate in Drosophila melanogaster. Cell Tissue Res. 273, 119–125.
Chase, R. (2002) Behavior and its neural control in gastropod molluscs. Oxford Univ. Press, New York.
Chiel, H. J., Weiss, K. R., Kupfermann, I. (1990) Multiple roles of a histaminergic afferent neuron in the feeding behavior of Aplysia. Trends Neurosci. 13, 223–227
Croll, R. P., Voronezhskaya, E. E. (1996) Early elements in gastropod neurogenesis. Dev. Biol. 173, 344–347.
Croll, R. P., Voronezhskaya, E. E., Hiripi, L., Elekes, K. (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: II. Postembryonic development of central and peripheral cells. J. Comp. Neurol. 404, 297–309.
Edvinsson, L., MacKenzie, E. T., McCullogh, J. (1993). Histamine. In: Edvinsson, L., MacKenzie, E. T., McCulloch, J. (eds), Cerebral blood flow and metabolism. Raven Press, New York, pp. 313–324.
Elekes, K., Kemenes, G., Hiripi, L., Geffard, M., Benjamin, P. R. (1991) Dopamine-immunoreactive neurones in the central nervous system of the pond snail Lymnaea stagnalis. J. Comp. Neurol. 307, 214–224.
Elekes, K., Voronezhskaya, E. E., Hiripi, L., Eckert, M., Rapus, J. (1996) Octopamine in the developing nervous system of the pond snail, Lymnaea stagnalis L. Acta Biol. Hung. 47, 73–87.
Elste, A., Koester, J., Shapiro, E., Panula, P., Schwartz, J. H. (1990) Identification of histaminergic cells in Aplysia. J. Neurophysiol. Vol. 64, No. 3. 736–744.
Hardie, R. C. (1987) Is histamine a neurotransmitter in insect photoreceptors? J. Comp. Physiol. 161A, 201–213.
Hardie, R. C. (1988) Effects of antagonists on putative histamine receptors in the first visual neuropil of the housefly (Musca domestica). J. Exp. Biol. 138, 221–241.
Hardie, R. C. (1989) A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339, 704–706.
Hegedűs, E., Kaslin, J., Hiripi, L., Kiss, T., Panula, P., Elekes, K. (2004) Histaminergic neurons in the central and peripheral nervous system of gastropods (Helix, Lymnaea): an immunocytochemical, biochemical and electrophysiological approach. J. Comp. Neurol. (in press).
Homberg, U., Hildebrand, J. G. (1991) Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of the sphinx moth Manduca sexta. J. Comp. Neurol. 307, 647–657.
Hough, L. B. (1988) Cellular localisation and possible functions for brain histamine: recent progress. Prog. Neurobiol 30, 469–505.
Kemenes, G., Elekes, K., Hiripi, L., Benjamin, P. R. (1989) A comparison of four techniques for mapping the distribution of serotonin and serotonin-containing neurons in fixed and living ganglia of the snail, Lymnaea. J. Neurocytology 18, 193–208.
Marois, R., Croll, R. P. (1992) Development of serotonin-like immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J. Comp. Neurol. 322, 255–265.
McCaman, R. E., Weinreich, D. (1985) Histaminergic synaptic transmission in the cerebral ganglion of Aplysia. J. Neurophysiol. 53, 1016–1037.
McClintock, T. S., Ache, B. W. (1989) Histamine directly gates a cloride channel in lobster olfactory receptor neurons. Proc. Natl. Acad. Sci. USA 86, 8137–8141.
Meshcheryakov, V. N. (1990) The common pond snail Lymnaea stagnalis L. In: Detlaff, D. A., Vassetzky, S. G. (eds) Animal species for developmental studies. Plenum Press, New York, London, pp. 69–132.
Morrill, J. B. (1982) Development of the pulmonate gastropod, Lymnaea. In: Harrison, F. W., Cowden, R. R. (eds) Developmental biology of freshwater invertebrates. Alan P. Liss, New York, pp. 399–483.
Mulloney, B., Hall, W. M. (1991) Neurons with histamine-like immunoreactivity in the segmental and stomatogastric nervous system of the crayfish Pacifastacus leniusculus and the lobster Homarus americanus. Cell Tissue Res. 266, 197–297.
Nässel, D. R., Pirvola, U., Panula, P. (1990) Histamine-like immunoreactive neurons innervating putative neurohemal areas and central neuropil in the thoracic-abdominal ganglia of the flies Drosophila and Calliphora. J. Comp. Neurol. 297, 525–536.
Nässel, D. R. (1999) Histamine in the brain of insects: a review. Micr. Res. Tech. 44, 121–136.
Panula, P., Karlstedt, T., Sallmen, T., Peitsaro, N., Kaslin, J., Michelsen, K. A., Anichtchik, O., Kukko-Lukjanov, T., Lintunen, M. (2000) The histaminergic system in the brain: structural characteristics and changes in hibernation. J. Chem. Neuroanat. 18, 65–74.
Panula, P., Yang, H. Y., Costa, E. (1984) Histamine-containing neurons in the rat hypothalamus. Proc. Natl. Acad. Sci. USA 81, 2572–2576.
Pirvola, U., Tuomisto, L., Yamatodani, A., Panula, P. (1988) Distribution of histamine in the cockroach brain and visual system: an immunocytochemical and biochemical study. J. Comp. Neurol. 276, 514–526.
Raven, C. P. (1966) Morphogenesis: The analysis of molluscan development. Pergamon Press, Oxford.
Schmid, A., Duncker, M. (1993) On the function of histamine in the central nervous system of Arthropods. Acta Biol. Hung. 44, 67–75.
Serfőző, Z., Elekes, K., Varga, V. (1998) NADPH-diaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis. Cell Tissue Res. 292, 579–586.
Serfőző, Z., Elekes, K. (2002) Nitric oxide level regulates the embryonic development of the pond snail Lymnaea stagnalis: pharmacological, behavioral, and ultrastructural studies. Cell Tissue Res. 310, 119–130.
Serfőző, Z., Veréb, Z., Rőszer, T., Kemenes, Gy., Elekes, K. (2002) Development of the nitric oxide/cGMP system in the embryonic and juvenile pond snail, Lymnaea stagnalis L. A comparative in situ hybridization, histochemical and immunohistochemical study. J. Neurocytology 31, 131–147.
Soinila, S., Mpitsos, G. J., Panula, P. (1990) Comparative study of histamine immunoreactivity in nervous systems of Aplysia and Pleurobranchaea. J. Comp. Neurol. 298, 83–96.
Vehovszky, Á., Elliott, C. H., Voronezhskaya, E. E., Hiripi, L., Elekes, K. (1998) Octopamine: a new feeding modulator in Lymnaea. Phil. Trans. Roy. Soc. B Lond. 353, 1631–1643.
Voronezhskaya, E. E., Elekes, K. (1993) Distribution of serotonin-like immunoreactive neurons in the embryonic nervous system of lymnaeid and planorbid snails. Neurobiology 1, 371–383.
Voronezhskaya, E. E., Elekes, K. (1996) Transient and sustained expression of FMRFamide-like immunoreactivity in the developing nervous system of Lymnaea stagnalis (Mollusca, Pulmonata). Cell. Mol. Neurobiol. 16, 661–676.
Voronezhskaya, E. E., Elekes, K. (2003) Expression of peptides encoded by the FMRFamide gene in the developing nervous system of Lymnaea stagnalis. Cell Tissue res. (in press).
Voronezhskaya, E. E., Hiripi, L., Elekes, K., Croll, R. P. (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopamine-containing neurons and dopamine-dependent behaviors. J. Comp. Neurol. 404, 285–296.
Willows, A. O. D. (1985) The Mollusca: Neurobiology and Behaviour. Part 1, Vol. 8, Academic Press, Orlando.
Willows, A. O. D. (1986) The Mollusca: Neurobiology and Behaviour. Part 2, Vol. 9, Academic Press, Orlando.
Yamatodani, A., Fukuda, H., Wada, H. (1985) High-performance liquid chromatographic determination of plasma and brain histamine without previous purification of biological samples: cation-exchange chromatography coupled with post-column derivatization fluorometry. J. Chromatography 344, 115–123.
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Presented at the 10th ISIN Symposium on Invertebrate Neurobiology, July 5–9, 2003, Tihany, Hungary.
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Hegedűs, E., Kaslin, J. & Elekes, K. Embryogenesis of the Histaminergic System in the Pond Snail, Lymnaea stagnalis L.: An Immunocytochemical and Biochemical Study. BIOLOGIA FUTURA 55, 301–313 (2004). https://doi.org/10.1556/ABiol.55.2004.1-4.36
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DOI: https://doi.org/10.1556/ABiol.55.2004.1-4.36