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Immunocytochemical demonstration of peptidergic and serotoninergic components in the enteric nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea)

  • D. J. A. Brownlee (a1), I. Fairweather (a1), C. F. Johnston (a2) and C. Shaw (a2)

Summary

The localization and distribution of neuropeptides and an indoleamine (serotonin or 5-hydroxytryptamine) in the enteric nervous system (ENS) of the pig roundworm, Ascaris suum, have been determined by the application of an indirect immunofluorescence technique in conjunction with confocal scanning laser microscopy. Whole-mount preparations of pharyngeal, intestinal and rectal regions were screened with antisera to 23 vertebrate peptides, 2 invertebrate peptides and serotonin (= 5-HT). Positive immunoreactivity (IR) was obtained with antisera to pancreatic polypeptide (PP), peptide YY (PYY), FMRFamide, gastrin and serotonin. The only IR observed in the ENS was that evident in the nerve supply to the pharynx and rectal region; no IR was associated with any region of the intestine. The most extensive patterns of IR occurred with antisera to PYY, FMRFamide and serotonin. In the pharyngeal component of the ENS, IR was evident in the lateral and dorsal longitudinal pharyngeal nerves, pharyngeal commissures, nerve plexus, and associated nerve cells and fibres. In contrast, the distribution of IR to the PP and gastrin antisera was more restricted and displayed a lower intensity of immunostaining. The other component of the ENS, the rectal enteric system, only yielded immunostaining to FMRFamide. The possible role of neuropeptides and serotonin in the nutritional biology of nematodes is discussed.

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Albertson, D. G. & Thomson, J. N. (1976). The pharynx of Caenorhabditis elegans. Philosophical Transactions of the Royal Society, B 275, 299325.
Atkinson, H. J., Isaac, R. E., Harris, P. D. & Sharpe, C. M. (1988). FMRFamide-like immunoreactivity within the nervous system of the nematodes Panagrellus redivivus, Caenorhabditis elegans and Heterodera glycines. Journal of Zoology 216, 663–71.
Avery, L. (1993). Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. Journal of Experimental Biology 175, 283–97.
Avery, L. & Horvitz, H. R. (1989). Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3, 473–85.
Avery, L. & Horvitz, H. R. (1990). Effects of Starvation and neuroactive drugs on feeding in Caenorhabditis elegans. Journal of Experimental Zoology 253, 263–70.
Banner, S. E. & Osborne, R. H. (1989). Modulation of 5-HT and proctolin receptors of FMRFamide in the foregut of the locust Schistocerca gregaria. Journal of Insect Physiology 35, 887–92.
Bird, A. F. (1971). The nervous system. In The Structure of Nematodes (ed. Bird, A. F.), pp. 130–70. New York: Academic Press.
Bone, L. W. & Bottjer, K. P. (1985). Stimulation of ingestion in Trichostrongylus colubriformis (Nematoda). Proceedings of the Helminthological Society of Washington 52, 80–4.
Brownlee, D. J. A., Fairweather, I., Johnston, C. F., Smart, D., Shaw, C. & Halton, D. W. (1993). Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea). Parasitology 106, 305–16.
Brownlee, D. J. A., Fairweather, I. & Johnston, C. F. (1993). Immunocytochemical demonstration of neuropeptides in the peripheral nervous system of the roundworm, Ascaris suum (Nematoda: Ascaroidea). Parasitology Research 79, 302–8.
Bullock, T. H. (1965). Pseudocoelomate Phyla: Acanthocephala, Rotifera, Gastrotricha, Kinorhyncha, Nematoda, Nematomorpha, and Entoprocta. In Structure and Function in the Nervous Systems of Invertebrates (ed. Bullock, T. H. & Horridge, G. A.), pp. 597629. San Francisco and London: W. H. Freeman and Company.
Chaudhuri, J. & Donahue, M. J. (1989). Serotonin receptors in the tissues of adult Ascaris suum. Molecular and Biochemical Parasitology 35, 191–8.
Chaudhuri, J., Martin, R. E. & Donahue, M. J. (1988). Evidence for the absorption and synthesis of 5-hydroxytryptamine in perfused muscle and intestinal tissue and whole worms of adult Ascaris suum. Parasitology 96, 157–70.
Chitwood, B. G. & Chitwood, M. B. (1974). The nervous system. In Introduction to Nematology (ed. Chitwood, B. G. & Chitwood, M. B.), pp. 160–74. Baltimore: University Park Press.
Coons, A. H., Leduc, E. H. & Connolly, J. M. (1955). Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. Journal of Experimental Medicine 102, 4960.
Cowden, C. & Stretton, A. O. W. (1993). AF2, an Ascaris neuropeptide: isolation, sequence and bioactivity. Peptides 14, 423–30.
Cowden, C., Stretton, A. O. W. & Davis, R. E. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73.
Croll, N. A. (1972). Behavioural activities of nematodes. Helminthological Abstracts 41A, 359–77.
Croll, N. A. (1975). Indolealkyamines in the coordination of nematode behavioral activities. Canadian Journal of Zoology 53, 894903.
Davenport, T. R. B., Lee, D. L. & Isaac, R. E. (1988). Immunocytochemical demonstration of a neuropeptide in Ascaris suum (Nematoda) using an antiserum to FMRFamide. Parasitology 97, 81–8.
Deineka, D. (1908). Das Nervensystem von Ascaris. Zeitschrift für wissenschaftliche Zoologie 89, 242307.
Di Maggio, D. A., Chronwall, B. M., Buchanan, K. & O'Donohue, T. L. (1985). Pancreatic polypeptide immunoreactivity in rat brain is actually neuropeptide Y. Neuroscience 15, 1149–57.
Donahue, M. J., Yacoub, N. J., Michnoff, C. A., Masaracchia, R. A. & Harris, B. G. (1981). Serotonin (5-hydroxytryptamine): a possible regulator of glycogenolysis in perfused muscle segments of Ascaris suum. Biochemical and Biophysical Research Communications 101, 112–17.
El-Salhy, M., Grimelius, L., Emson, P. C. & Falkmer, S. (1987). Polypeptide YY- and neuropeptide Y-immunoreactive cells and nerves in the endocrine and exocrine pancreas of some vertebrates: an onto- and phylogentic study. Histochemistry Journal 119, 111–17.
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in platyhelminths. Parasitology 102, S77S92.
Geary, T. G., Klein, R. D., Vanover, L., Bowman, J. W. & Thompson, D. P. (1992 a). The nervous systems of helminths as targets for drugs. Journal of Parasitology 78, 215–30.
Geary, T. G., Price, D. A., Bowman, J. W., Winterrowd, C. A., Mackenzie, C. D., Garrison, R. D., Williams, J. F. & Friedman, A. R. (1992 b). Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–14.
Goh, S. L. & Davey, K. G. (1976). Selective uptake of noradrenaline, DOPA, and 5-hydroxytryptamine by the nervous system of Phocanema decipiens (Nematoda): a light autoradiographic and ultrastructural study. Tissue and Cell 8, 421–35.
Goh, S. L. & Davey, K. G. (1985). Occurrence of noradrenaline in the central nervous system of Phocanema decipiens and its possible role in the control of ecdysis. Canadian Journal of Zoology 63, 475–9.
Goldschmidt, R. (1910). Das Nervensystem von Ascaris lumbricoides und megalocephala. Festschrift für R Hertwigs 2, 253354.
Harpur, R. P. (1964). Maintenance of Ascaris lumbricoides in vitro III. Changes in the hydrostatic skeleton. Comparative Biochemistry and Physiology 13, 7185.
Holden-Dye, L. & Walker, R. J. (1990). Avermectin and avermectin derivatives are antagonists at the 4-aminobutyric acid (GABA) receptor on the somatic muscle cells of Ascaris; is this the site of anthelmintic action? Parasitology 101, 265–71.
Horvitz, H. R., Chalfie, M., Trent, C., Sulston, J. E. & Evans, P. D. (1982). Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216, 1012–14.
Hutchinson, G. W. & Probert, A. J. (1972). Ascaris suum: kinetic properties, tissue specificity and ultrastructural location of cholinesterases. Experimental Parasitology 32, 109–16.
Jennings, J. B. & Colam, J. B. (1970). Gut Structure, digestive physiology and food storage in Pontonema vulgaris (Nematoda: Enoplida). Journal of Zoology 161, 211–21.
Johnson, C. D. & Stretton, A. O. W. (1987). GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. Journal of Neuroscience 7, 223–35.
Johnston, C. F., Shaw, C., Halton, D. W. & Fairweather, I. (1990). Confocal scanning laser microscopy and helminth neuroanatomy. Parasitology Today 6, 305–8.
Krajniak, K. G. & Greenberg, M. J. (1992). The localization of FMRFamide in the nervous and somatic tissues of Nereis virens and its effects upon the isolated esophagus. Comparative Biochemistry and Physiology 101C, 93100.
Krajniak, K. G., Greenberg, M. J., Price, D. A., Doble, K. E. & Lee, T. D. (1989). The identification, localization, and pharmacology of FMRFamide-related peptides and SCPB in the penis and crop of the terrestrial slug, Limax maximus. Comparative Biochemistry and Physiology 94C, 485–92.
Leach, L., Trudgill, D. L. & Gahan, P. B. (1987). Immunocytochemical localization of neurosecretory amines and peptides in the free-living nematode, Goodeyus ulmi. Histochemical Journal 19, 471–5.
Lee, D. L. (1962). The distribution of esterase enzymes in Ascaris lumbricoides. Parasitology 52, 241–60.
Lee, D. L. & Ko, R. C. (1991). Catecholaminergic neurons in Trichinella spiralis (Nematoda). Parasitology Research 77, 269–70.
Lehman, H. K. & Greenberg, M. J. (1987). The actions of FMRFamide-like peptides on visceral and somatic muscles of the snail Helix aspersa. Journal of Experimental Biology 131, 5568.
Lent, C. M. & Dickinson, M. H. (1988). The neurobiology of feeding in leeches. Scientific American 258, 7883.
Li, C. & Chalfie, N. (1986). FMRFamide-like immunoreactivity in C. elegans. Society of Neuroscience Abstracts 12, 246.
Lui, A., Bečejac, S., Krvavica, S. & Ćorić, D. (1963). On the activity and localization of cholinesterase in Ascaris suum Goetz. Veterinarski arhiv 33, 307–11.
Martin, R. E. & Donahue, M. J. (1989). Tissue and ultrastructural localisation of 5-hydroxytryptaniine (serotonin) in the tissues of Ascaris suum with energy dispersive X-ray spectrometry of immunoreactive structures. International Journal for Parasitology 19, 585–96.
Martin, R. J., Pennington, A. J., Duittoz, A. H., Robertson, S. & Kusel, J. (1991). The physiology and pharmacology of neuromuscular transmission in the nematode parasite, Ascaris suum. Parasitology 102, 541–58.
Mishra, S. K., Sen, R. & Ghatak, S. (1984). Ascaris lumbricoides and Ascaridia galli: biogenic amines in adults and developmental stages. Experimental Parasitology 57, 34–9.
Phillips, J. L., Sturman, G. & West, G. B. (1975). The presence of histamine in the tissues of Ascaris suum. General Pharmacology 6, 295–7.
Rosoff, M. L., Doble, K. E., Price, D. A. & Li, C. (1993). The flp-1 propeptide is processed into multiple, highly similar FMRFamide-like peptides in Caenorhabditis. Peptides 14, 331–8.
Schinkmann, K. & Li, C. (1992). Localization of FMRFamide-like peptides in Caenorhabditis elegans. Journal of Comparative Neurology 316, 251–60.
Sharpe, M. J. & Atkinson, H. J. (1980). Improved visualization of dopaminergic neurons in nematodes using the glyoxylic acid fluorescence method. Journal of Zoology 190, 273–84.
Sithigorngul, P., Stretton, A. O. W. & Cowden, C. (1990). Neuropeptide diversity in Ascaris: an immunocytochemical study. Journal of Comparative Neurology 294, 362–76.
Smart, D., Shaw, C., Johnston, C. F., Halton, D. W., Fairweather, I. & Buchanan, K. D. (1992). Chromatographic and immunological characterisation of immunoreactivity towards pancreatic polypeptide and neuropeptide Y in the nematode Ascaris suum. Comparative Biochemistry and Physiology 102C, 477–81.
Stretton, A. O. W. (1992). Chemical intercellular signalling mechanisms in the nervous system of the nematode Ascaris suum: potential sites of actions of new generations of anthelmintic drugs. In Neurotox 91. Molecular Basis of Drug and Pesticide Action (ed. Duce, I. A.), pp. 123–38. Amsterdam: Elsevier Applied Science.
Sulston, J., Dew, M. & Brenner, S. (1975). Dopaminergic neurons in the nematode Caenorhabditis elegans. Journal of Comparative Neurology 163, 215–26.
Turner, M. J. & Schaeffer, J. M. (1989). Mode of action of ivermectin. In Ivermectin and Abamectin (ed. Campbell, W. C.), pp. 7388. New York, Berlin, Heidelberg: Springer-Verlag.
Wann, K. T. (1987). The cellular actions of the avermectins. Phytotherapy Research 1, 143–50.
Ward, S., Thomson, N., White, J. G. & Brenner, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. Journal of Comparative Neurology 160, 313–38.
Willett, J. D. (1980). Control mechanisms in nematodes. In Nematodes and Biological Models, vol. 1, Behavioral and Developmental Models (ed. Zuckerman, B. M.), pp. 197225. New York: Academic Press.
Williams, J. A., Shahkolahi, A. M., Abbassi, M. & Donahue, M. J. (1992). Identification of a novel 5-HTN (Nematoda) receptor from Ascaris suum muscle. Comparative Biochemistry and Physiology 101C, 469–74.

Keywords

Immunocytochemical demonstration of peptidergic and serotoninergic components in the enteric nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea)

  • D. J. A. Brownlee (a1), I. Fairweather (a1), C. F. Johnston (a2) and C. Shaw (a2)

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