Hostname: page-component-f554764f5-rvxtl Total loading time: 0 Render date: 2025-04-13T17:00:35.183Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda: Ascaroidea)

Published online by Cambridge University Press:  06 April 2009

D. J. A. Brownlee ,
I. Fairweather ,
C. F. Johnston ,
D. Smart ,
C. Shaw  and
D. W. Halton
D. J. A. Brownlee
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
I. Fairweather*
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
C. F. Johnston
Affiliation:
Comparative Neuroendocrinology Research Group, School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
D. Smart
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
C. Shaw
Affiliation:
Comparative Neuroendocrinology Research Group, School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
D. W. Halton
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland
*
*Dr I. Fairweather, School of Biology and Biochemistry, The Queen's University of Belfast, Medical Biology Centre, Belfast BT9 7BL, Northern Ireland
Get access Rights & Permissions [Opens in a new window]

Summary

The localization and distribution of neuropeptides in the central nervous system of the pig roundworm, Ascaris suum, have been determined by an indirect immunofluorescence technique in conjunction with confocal microscopy. Antisera to 25 vertebrate peptides and two invertebrate peptides were used to screen the worm for immunoreactivity (IR). Immuno-staining was obtained with antisera to pancreatic polypeptide (PP), peptide YY (PYY), neuropeptide Y (NPY), gastrin, cholecystokinin (CCK), substance P (SP), atrial natriuretic peptide (ANP), salmon gonadotropin-releasing hormone (SGnRH), mammalian gonadotropin-releasing hormone (MGnRH), chromogranin A (CGA) and FMRFamide. The most extensive patterns of IR occurred with antisera to PYY, FMRFamide and gastrin. IR was evident in nerve cells and fibres in the ganglia associated with the anterior nerve ring and in the main nerve cords and their commissures; IR to FMRFamide also occurred in the posterior nerve ring. Immunostaining for the other peptides was confined to the nerve cords, with the number of immunoreactive nerve fibres varying from peptide to peptide.

Keywords

Ascaris suumNematodaneuropeptidesimmunocytochemistryconfocal microscopy
Type
Research Article
Information
Parasitology , Volume 106 , Issue 3 , April 1993 , pp. 305 - 316
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

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.CrossRefGoogle Scholar
Barker, G. C. & Rees, H. (1990). Ecdysteroids in nematodes. Parasitology Today 6, 384–7.CrossRefGoogle ScholarPubMed
Basch, P. F. & Gupta, B. C. (1988). Immunocytochemical localization of regulatory peptides in six species of trematode parasites. Comparative Biochemistry and Physiology 91C, 565–70.Google ScholarPubMed
Brenner, B. M., Ballermann, B. J., Gunning, M. E. & Zeidel, M. L. (1990). Diverse biological actions of atrial natriuretic peptide. Physiological Reviews 70, 665–99.CrossRefGoogle ScholarPubMed
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. 597–629. San Francisco and London: W. H. Freeman.Google Scholar
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.Google Scholar
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, 49–60.CrossRefGoogle Scholar
Cottrell, G. A. (1989). The biology of the FMRFamide-series of peptides in molluscs with special reference to Helix. Comparative Biochemistry and Physiology 93A, 41–5.CrossRefGoogle ScholarPubMed
Cowden, C. & Stretton, A. O. W. (1990). AF2, a nematode neuropeptide. Neuroscience 16, 305.Google Scholar
Cowden, C., Stretton, A. O. W. & Davis, R. E. (1989). AFl, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73.CrossRefGoogle Scholar
Curry, W. J., Fairweather, I., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1989). Immunocytochemical demonstration of vertebrate neuropeptides in the earthworm Lumbricus terrestris (Annelida, Oligochaeta). Cell and Tissue Research 257, 577–86.CrossRefGoogle Scholar
Curry, W. J., Shaw, C., Johnston, C. F., Thim, L. & Buchanan, K. D. (1991). Isolation and characterisation of neuropeptide F from the turbellarian Artioposthia triangulata. Regulatory Peptides 35, 231.Google Scholar
Davenport, T. R. B., Isaac, R. E. & Lee, D. L. (1991). The presence of peptides related to the adipokinetic hormone/red pigment concentrating hormone family in the nematode, Panagrellus redivivus. General and Comparative Endocrinology 81, 419–25.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Davey, K. G. (1964). Neurosecretory cells in a nematode, Ascaris lumbricoides. Canadian Journal of Zoology 42, 731–4.CrossRefGoogle Scholar
Davey, K. G. (1966). Neurosecretion and molting in some parasitic nematodes. American Zoologist 6, 243–9.CrossRefGoogle ScholarPubMed
Davey, K. G. (1988). Endocrinology of Nematodes. In Invertebrate Endocrinology, vol. 2, Endocrinology of Selected Invertebrate Types (ed. Downer, R. G. H. & Laufer, H.), pp. 63–86. New York: Alan R. Liss.Google Scholar
De Loop, A. & Schoofs, L. (1990). Homologies between the amino acid sequences of some vertebrate peptide hormones and peptides isolated from invertebrate sources. Comparative Biochemistry and Physiology 95B, 459–68.Google Scholar
Delves, C. J., Webb, R. & Howells, R. E. (1989). Neurosecretory-like material in 3rd- and 4th-stage Dirofilaria immitis larvae (Nematoda: Filarioidea). Parasitology 99, 99–104.CrossRefGoogle Scholar
Dhainaut-Courtois, N., Tramu, G., Marcel, R., Malécha, J., Verger-Bocquet, M., Andries, J. C., Masson, M., Selloum, L., Belemtougri, G. & Beauvillain, J. C. (1985). Cholecystokinin in the nervous systems of invertebrates and protochordates. Immunohistochemical localization of a cholecystokinin-8-like substance in annelids and insects. Annals of the New York Academy of Sciences 448, 167–87.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Elphick, M. R., Price, D. A., Lee, T. D. & Thorndyke, M. C. (1991). The SALMFamides: a new family of neuropeptides isolated from an echinoderm. Proceedings of the Royal Society of London, B 243, 121–7.Google ScholarPubMed
Evans, B. D., Pohl, J., Kartsonis, N. A. & Calabrese, R. L. (1991). Identification of RFamide neuropeptides in the medicinal leech. Peptides 12, 897–908.CrossRefGoogle ScholarPubMed
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in platyhelminths. Parasitology 102, S77–S92.CrossRefGoogle ScholarPubMed
Fairweather, I., Halton, D. W. & Shaw, C. (1992). Regulatory peptides in host-parasite interactions; characterisation and roles in pathophysiology and immune responses. Advances in Neuroimmunology 2, 249–65.CrossRefGoogle Scholar
Goldschmidt, R. (1909). Das Nervensystem von Ascaris lumbricoides und Megalocephala. II. Ein Versuch, in den Aufbau eines einfachen Nervensystems einzudringen. Zeitschrift für wissenschaftliche Zoologie 92, 306–57.Google Scholar
Grimmelikhuijzen, C. J. P., Graff, D. & McFarlane, I. D. (1989). Neurones and neuropeptides in coelenterates. Archives of Histology and Cytology 52 (Supp1.), 265–76.CrossRefGoogle ScholarPubMed
Halton, D. W., Shaw, C., Maule, A. G., Johnston, C. F. & Fairweather, I. (1992). Peptidergic messengers: a new perspective of the nervous system of parasitic platyhelminths. Journal of Parasitology 78, 179–93.CrossRefGoogle ScholarPubMed
Holman, G. M., Nachman, R. J. & Wright, M. S. (1990). Insect neuropeptides. Annual Review of Entomology 35, 201–17.CrossRefGoogle ScholarPubMed
Iversen, L. L. (1987). Overview: peptides in the nervous system. In Neuropeptides and Their Peptidases (ed. Turner, A. J.), pp. 3–8. Chichester: Ellis Horwood Ltd.Google Scholar
Jensen, J. (1989). Substance P and other tachykinins. In The Comparative Physiology of Regulatory Peptides (ed. Holmgren, S.), pp. 130–49. London: Chapman and Hall Ltd.CrossRefGoogle Scholar
Johnson, C. D. & Stretton, A. O. W. (1980). Neural control of locomotion in Ascaris: anatomy, electrophysiology, and biochemistry. In Nematodes as Biological Models (ed. Zuckerman, B. M.), Vol. 1, pp. 159–95. London: Academic Press.Google Scholar
Johnson, C. D. & Stretton, A. O. W. (1985). Localization of choline acetyltransferase within identified motorneurons of the nematode Ascaris. Journal of Neuroscience 5, 1984–92.CrossRefGoogle Scholar
Johnson, C. D. & Stretton, A. O. W. (1987). GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris. Journal of Neuroscience 7, 223–35.CrossRefGoogle ScholarPubMed
Jönsson, A.-C. (1989). Gastrin/cholecystokinin-related peptides-comparative aspects. In The Comparative Physiology of Regulatory Peptides (ed. Holmgren, S.), pp. 61–86. London: Chapman and Hall Ltd.CrossRefGoogle Scholar
Kaloustian, K. V. & Edmands, J. A. (1986). Immunochemical evidence for substance P-like peptide in tissues of the earthworm Lumbricus terrestris: action on intestinal contraction. Comparative Biochemistry and Physiology 83C, 329–33.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Le Roith, D. & Roth, J. (1984). Evolutionary origins of messenger peptides: materials in microbes that resemble vertebrate hormones. In Evolution and Tumour Pathology of the Neuroendocrine System (ed. Falkmer, S., Håkanson, R. & Sundler, F.), pp. 147–64. Amsterdam: Elsevier Science Publishers B.V.Google Scholar
Linacre, A., Kellett, E., Saunders, S., Bright, K., Benjamin, P. R. & Burke, J. F. (1990). Cardioactive neuropeptide Phe-Met-Arg-Phe-NH2 (FMRFamide) and novel related peptides are encoded in multiple copies by a single gene in the snail Lymnaea stagnalis. Journal of Neuroscience 10, 412–19.CrossRefGoogle ScholarPubMed
Maggio, J. E. (1988). Tachykinins. Annual Review of Neurosciences 11, 13–28.CrossRefGoogle ScholarPubMed
Martin, R. E. & Donahue, M. J. (1989). Tissue and ultrastructural localization of 5-hydroxytryptamine (serotonin) in the tissues of Ascaris suum with energy dispersive X-ray spectrometry of immunoreactive structures. International Journal for Parasitology 19, 585–96.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Thim, L., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1991). Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology 102, 309–16.CrossRefGoogle Scholar
Millar, R. P. & King, J. A. (1988). Evolution of gonadotropin-releasing hormone: multiple usage of a peptide. News in Physiological Sciences 3, 49–53.Google Scholar
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.CrossRefGoogle ScholarPubMed
O'hanlon, G. M., Cleator, M., Mercer, J. G., Howells, R. E. & Rees, H. H. (1991 a). Metabolism and fate of ecdysteroids in the nematodes Ascaris suum and Parascaris equorum. Molecular and Biochemical Parasitology 47, 179–88.CrossRefGoogle ScholarPubMed
O'hanlon, G. M., Mercer, J. G. & Rees, H. H. (1991 b). Evidence for the release of 20-hydroxyecdysone 25- glucoside by adult female Parascaris equorum (Nematoda) in vitro. Parasitology Research 11, 271–2.CrossRefGoogle Scholar
Phillips, J. L., Sturman, G. & West, G. B. (1975). The presence of histamine in the tissues of Ascaris suum. General Pharmacology 6, 295–7.CrossRefGoogle Scholar
Pierobon, P., Kemali, M. & Milici, N. (1989). Substance P and Hydra: an immunohistochemical and physiological study. Comparative Biochemistry and Physiology 92C, 217–21.Google ScholarPubMed
Rosenzweig, A. & Seidman, C. E. (1991). Atrial natriuretic factor and related peptide hormones. Annual Review of Biochemistry 60, 229–55.CrossRefGoogle ScholarPubMed
Roth, J., Le Roith, D., Lesniak, M. A., De Pablo, F., Bassas, L. & Collier, E. (1986). Molecules of intercellular communication in vertebrates, invertebrates and microbes: do they share common origins? Progress in Brain Research 68, 71–9.CrossRefGoogle ScholarPubMed
Sithigorngul, P., Stretton, A. O. W. & Cowden, C. (1990). Neuropeptide diversity in Ascaris: an immunocytochemical study. Journal of Comparative Neurology 294, 362–76.CrossRefGoogle ScholarPubMed
Skuce, P. J., Johnston, C. F., Fairweather, I., Halton, D. W., Shaw, C. & Buchanan, K. D. (1990 a). Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke, Schistosoma mansoni. Cell and Tissue Research 261, 573–81.CrossRefGoogle Scholar
Skuce, P. J., Johnston, C. F., Shaw, C., Millar, R. P., Fairweather, I. & Halton, D. W. (1990 b). Immunoreactivity to gonadotropin releasing hormone in adult Schistosoma mansoni. Bulletin de la Société Française de Parasitologie 8 (Suppl.), 113.Google Scholar
Stretton, A. O. W., Cowden, C., Sithigorngul, P. & Davis, R. E. (1991). Neuropeptides in the nematode Ascaris suum. Parasitology 102, S107–S116.CrossRefGoogle ScholarPubMed
Sulston, J., Dew, M. & Brenner, S. (1975). Dopaminergic neurons in the nematode Caenorhabditis elegans. Journal of Comparative Neurology 163, 215–26.CrossRefGoogle ScholarPubMed
Taghert, P. H. & Schneider, L. E. (1990). Interspecific comparison of a Drosophila gene encoding FMRFamide-related neuropeptides. Journal of Neuroscience 10, 1929–42.CrossRefGoogle ScholarPubMed
Thorndyke, M. C. (1986). Immunocytochemistry and evolutionary studies with particular reference to peptides. In Immunocytochemistry, Modern Methods and Applications 2nd Edn (ed. Polak, J. M. & van Noorden, S.), pp. 308–27. Bristol: John Wright and Sons Ltd.Google Scholar
Vigna, S. R. (1986). Evolution of hormone and receptor diversity: cholecystokinin and gastrin. American Zoologist 26, 1033–40.CrossRefGoogle Scholar
Yang, H.-Y. T. & Majane, E. A. (1990). Mammalian Phe-Met-Arg-Phe-NH2-like peptides: structure, biological activity and distribution. Progress in Clinical and Biological Research 342, 86–91.Google ScholarPubMed