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Role of regulatory peptides in parasitic platyhelminths and their vertebrate hosts: possible novel factors in host-parasite interactions

Published online by Cambridge University Press:  06 April 2009

C. Shaw
Affiliation:
Department of Medicine, The Queen's University of Belfast, Belfast BT7 1NN
C. F. Johnston
Affiliation:
Department of Medicine, The Queen's University of Belfast, Belfast BT7 1NN

Extract

The study of regulatory peptides has its origins in the classical work of Bayliss & Starling (1902). Their pioneering work on the presence of a factor in intestinal extracts which, when injected into the bloodstream of experimental animals, elicited pancreatic secretion, led to the genesis of the concept of the hormone, i.e. a chemical messenger which is released from one part of the body in response to a stimulus to travel in the bloodstream to a distant target tissue where it would elicit a physiological response appropriate to the original stimulus. In keeping with accepted scientific tradition, this concept had its critics. Pavlov, who had been studying secretory stimulation from a different perspective, concluded from his work on salivation in dogs, that this was mediated via neural pathways. With hindsight, and the benefits of knowledge obtained from nearly a century of scientific research, we now know that these pioneers were in actual fact studying different aspects of the same process and that both theories were complementary. In fact, it is becoming increasingly difficult to ascribe secretory control to either circulating or neuronal factors as both appear to be intimately involved in regulation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

Ballesta, J., Bloom, S. R. & Polak, J. M. (1985). Distribution and localization of regulatory peptides. CRC Critical Reviews of Clinical Laboratory Science 22, 185218.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
Bayliss, W. M. & Starling, E. H. (1902). The mechanism of pancreatic secretion. Journal of Physiology 28, 325–53.CrossRefGoogle ScholarPubMed
Bryant, C. & Behm, C. A. (1989). Biochemical Adaptation of Parasites. London, New York: Chapman and Hall.Google Scholar
Bryant, M. G. & Bloom, S. R. (1982). Measurement in tissue. In Radioimmunoassay of Gut Regulatory Peptides (ed. Bloom, S. R. & Long, R. G.), pp. 3641. London, Philadelphia, Toronto: W. D. Saunders.Google Scholar
Bullock, T. H. (1965). Platyhelminths. In Structure and Function of the Nervous Systems of Invertebrates (ed. Bullock, T. H. & Horridge, G. A.), pp. 536577. San Francisco, London: W. H. Freeman.Google Scholar
Bullock, T. H. (1984). Comparative neuroscience holds promise for quiet revolutions. Science 225, 473–8.CrossRefGoogle ScholarPubMed
Chiu, A. Y., Hunkapiller, M. W., Heller, E., Stuart, D. K., Hood, L. E. & Strumwasser, F. (1979). Neuropeptide egg-laying hormone of Aplysia: purification and primary structure. Proceedings of the National Academy of Sciences, USA 76, 6656–60.CrossRefGoogle ScholarPubMed
Conlon, J. M., Deacon, C. F., O'Toole, L. & Thim, L. (1986). Scyliorhinin I and II: two novel tachykinins from dogfish gut. FEBS Letters 200, 111–16.CrossRefGoogle ScholarPubMed
Du, B.-H., Eng, J., Hulmes, J. D., Chang, M., Pan, Y.-C. E. & Yalow, R. S. (1985). Guinea pig has a unique mammalian VIP. Biochemical and Biophysical Research Communications 128, 1083–8.CrossRefGoogle Scholar
Ebberink, R. H. M., Loenhout, H.Van, Geraerts, W. P. M. & Joosse, J. (1985). Purification and amino acid sequence of the ovulation hormone of Lymnaea stagnalis. Proceedings of the National Academy of Sciences, USA 82, 7767–71.CrossRefGoogle ScholarPubMed
Erspamer, V. & Anastasia, A. (1962). Structure and pharmacological actions of eledoisin, the active undecapeptide of the posterior salivary glands of Eledone. Experientia 18, 58–9.CrossRefGoogle Scholar
Erspamer, V. (1981). The tachykinin peptide family. Trends in Neuroscience 4, 267–9.CrossRefGoogle Scholar
Erspamer, V., Anastasia, A., Bertaccini, B. & Cei, J. M. (1964). Structure and pharmacological actions of physalaemin, the main active polypeptide of the skin of Physalaemus fuscomaculatus. Experientia 20, 489–90.CrossRefGoogle Scholar
Erspamer, V., Erspamer, G. F. & Cei, J. M. (1986). Active peptides in the skin of two hundred and thirty American amphibian species. Comparative Biochemistry and Physiology 85C, 125–37.Google ScholarPubMed
Erspamer, V. & Melchiorri, p. (1980). Active polypeptides: from amphibian skin to gastrointestinal tracts and brain of mammals. Trends in Pharmaceutical Science 1, 391–3.CrossRefGoogle Scholar
Fairweather, I., Macartney, G. A., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1988). Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) and vertebrate neuropeptides in the nervous system of excysted cysticercoid larvae of the rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitology Research 47, 371–9.CrossRefGoogle Scholar
Fairweather, I., Mahendrasingam, S., Johnston, C. F., Halton, D. W. & Shaw, C. (1990). Peptidergic nerve elements in three developmental stages of the tetraphyllidean tapeworm, Trilocularia acanthiaevulgaris: an immunocytochemical study. Parasitology Research 76, 497508.CrossRefGoogle ScholarPubMed
Falkmer, S., El-Salhy, M. & Titlbach, M. (1984). Evolution of the neuroendocrine system in vertebrates. A review with particular reference to the phylogeny and postnatal maturation of the islet parenchyma. In Evolution and Tumour Pathology of the Neuroendocrine System (ed. Falkmer, S., Hakanson, R. & Sundler, F.), pp. 5987. Amsterdam, New York, Oxford: Elsevier.Google Scholar
Frontali, N. & Gainer, H. (1977). Peptides in invertebrate nervous systems. In Peptides in Neurobiology (ed. Gainer, H.), pp. 259294. New York, London: Plenum Press.CrossRefGoogle Scholar
Goldberg, D., Nusbaum, M. P. & Marder, E. (1988). Substance P-like immunoreactivity in the stomatogastric nervous systems of the crab Cancer borealis and the lobsters Panurilus interruptus and Homarus americanus. Cell and Tissue Research 252, 515–22.CrossRefGoogle Scholar
Greenberg, M. J. & Price, D. A. (1983). Invertebrate neuropeptides: native and naturalised. Annual Review of Physiology 45, 271–88.CrossRefGoogle Scholar
Gustafsson, M. (1985). Cestode neurotransmitters. Parasitology Today 1, 72–5.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. (1987). Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitology Research 74, 168–74.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. & Wikgren, M. C. (1989). Development of immunoreactivity to the nvertebrate neuropeptide small cardiac peptide B in the tapeworm Diphyllobothrium dendriticum. Parasitology Research 75, 396400.CrossRefGoogle Scholar
Halton, D. W. & Morris, G. P. (1969). Occurrence of cholinesterase and ciliated sensory structures in a fish-gill fluke, Diclidophora merlangi (Trematoda: Monogenea). Zeitschrift für Parasitenkunde 33, 2130.CrossRefGoogle Scholar
Haynes, L. W. (1980). Peptide neuroregulators in invertebrates. Progress in Neurobiology 15, 205–45.CrossRefGoogle ScholarPubMed
Howell, M. J. (1985). Gene exchange between hosts and parasites. International Journal for Parasitology 15, 597600.CrossRefGoogle ScholarPubMed
Itoh, N., Obata, K., Yanaihara, N. & Okamoto, T. (1983). Human preprovasoactive intestinal polypeptide contains a novel PHI-27 like peptide. Nature, London 304, 547–9.CrossRefGoogle ScholarPubMed
Kaloustian, K. V. & Edmands, J. A. (1986). Immunochemical evidence for a substance P-like peptide in tissues of the earthworm Lumbricus terrestris: action on intestinal contraction. Comparative Biochemistry and Physiology 83C, 329–33.Google ScholarPubMed
Magee, R. M., Fairweather, I., Johnston, C. F., Halton, D. W. & Shaw, C. (1989). Immunocytochemical demonstration of neuropeptides in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology 98, 227–38.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1989 a). Immunocytochemical demonstration of neuropeptides in the fish-gill parasite, Diclidophora merlangi (Monogenoidea). International Journal for Parasitology 19, 307–16.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F. & Fairweather, I. (1989 b). Localization, quantification, and characterization of pancreatic polypeptide immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host (Merlangius merlangus). General and Comparative Endocrinology 74, 50–6.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990 a). A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system in the monogenean parasite, Diclidophora merlangi. Parasitology Research 76, 409–19.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1990 b). Tachykinin immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host the whiting (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera. Comparative Biochemistry and Physiology 94C, 533–41.Google Scholar
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F. & Fairweather, I. (1990 c). Distribution and immunochemical characteristics of a neuropeptide in Moniezia expansa. Bulletin de la Société Française de Parasitologie 8, Suppl. 1, 109.Google Scholar
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F., Fahrenkrug, J., Fairweather, I. & Buchanan, K. D. (1990 d). VIP- and PHI-immunoreactive peptides in the tapeworm, Moniezia expansa: chromatographic co-elution with ovine (host) and porcine analogues. Regulatory Peptides 30, 48.CrossRefGoogle Scholar
McKay, D. M., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1990). Occurrence and distribution of putative neurotransmitters in the frog-lung parasite Haplometra cylindracea (Trematoda: Digenea). Parasitology Research 76, 509–17.CrossRefGoogle ScholarPubMed
McKay, D. M., Shaw, C., Halton, D. W., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1990). Mammalian regulatory peptide immunoreactivity in the trematode parasite Haplometra cylindracea and the lung of its frog host, Rana temporaria: comparative chromatographic characterisation using reverse phase high performance liquid chromatography. Comparative Biochemistry and Physiology 96C, 345–51.Google ScholarPubMed
McKillop, J. M., Foy, W. L., Johnston, C. F., Shaw, C., Murphy, R. F. & Buchanan, K. D. (1988). Identification and characterisation of gastrin-releasing peptide in the rat retina. Brain Research 447, 239–45.CrossRefGoogle Scholar
Nilsson, A. (1974). Isolation, amino acid composition and terminal amino acid residues of the vasoactive octacosapeptide from chicken intestine. Partial purification of chicken secretion. FEBS Letters 47, 284–9.CrossRefGoogle Scholar
O'Hare, M. M. T., Huda, I., Sloan, J. M., Kennedy, T. L. & Buchanan, K. D. (1985). Multiple immunoreactive forms of pancreatic polypeptide (PP) in islet cell tumours. Cancer 55, 1895–8.3.0.CO;2-S>CrossRefGoogle Scholar
Pearse, A. G. E. (1968). Histochemistry. Theoretical and Applied, vol. 1, Edinburgh, London and New York: Churchill Livingstone.Google 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
Platt, N. & Reynolds, S. E. (1988). Invertebrate neuropeptides. In Comparative Invertebrate Neurochemistry (ed. Lunt, G. G. & Olsen, R. W.), pp. 175226. Beckenham: Croom Helm.CrossRefGoogle Scholar
Rahemo, Z. I. F. & Gorges, N. S. (1987). Studies on the nervous system of Polystoma integerrium as revealed by acetylthiocholine activity. Parasitology Research 73, 234–9.CrossRefGoogle Scholar
Redmond, A. O. B., Buchanan, K. D. & Trimble, E. R. (1977). Insulin and glucagon response to arginine infusion in cystic fibrosis. Acta Paediatrica Scandia 66, 199204.CrossRefGoogle ScholarPubMed
Reuter, M. (1987). Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system of Gyrodactylus salaris (Monogenea). Acta Zoologica 68, 187–93.CrossRefGoogle Scholar
Reuter, M. (1988). Development and organisation of nervous systems visualised by immunocytochemistry in three flatworm species. Progress in Zoology 36, 181–4.Google Scholar
Reuter, M., Lehtonen, M. & Wikgren, M. (1988). Immunocytochemical evidence of neuroactive substances in flatworms of different taxa — a comparison. Acta Zoologica 69, 2937.CrossRefGoogle Scholar
Rohde, K. (1972). Ultrastructure of the nerves and sense receptors of Polystomoides renshi Rohde and P. malyi Rohde (Monogenea). Zeitschrift für Parasitenkunde 40, 307–20.CrossRefGoogle Scholar
Skuce, P. J., Johnston, C. F., Fairweather, I., Halton, D. W., Shaw, C. & Buchanan, K. D. (1990). 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
Smyth, J. D. & Halton, D. W. (1983). The Physiology of Trematodes, 2nd Edn. Cambridge: Cambridge University Press.Google Scholar
Smyth, J. D. & McManus, D. P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Straus, E. & Yalow, R. S. (1979). Gastrointestinal peptides in the brain. Federation Proceedings 38, 2320–4.Google ScholarPubMed
Sukhdeo, M. V. K. (1990). Habitat selection by helminths: a hypothesis. Parasitology Today 6, 234–7.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour: understanding platyhelminth responses. Advances in Parasitology 26, 73144.CrossRefGoogle ScholarPubMed
Tatemoto, K., Carlquist, M. & Mutt, V. (1982). Neuropeptide Y - a novel brain peptide with structural similarities to peptide tyrosine tyrosine and pancreatic polypeptide. Nature, London 296, 659–60.CrossRefGoogle Scholar
Thwaites, D. T., Dimaline, R., Moore, S. J. & Thorndyke, M. C. (1990). Tissue distribution, molecular forms, and cellular origins of dogfish VIP demonstrated using region-specific antisera. Regulatory Peptides 30, 58.CrossRefGoogle Scholar
Noorden, S.Van & Falkmer, S. (1980). Gut-islet endocrinology – some evolutionary aspects. Investigative Cell Pathology 3, 2135.Google ScholarPubMed
Noorden, S.Van & Polak, J. M. (1983). Immunocytochemistry today: techniques and practice. In Immunocytochemistry – Practical Applications in Pathology and Biology (ed. Polak, J. M. & Noorden, S.Van), pp. 1142. Bristol, London, Boston: Wright PSG.Google Scholar
Walker, R. J. & Holden-Dye, L. (1989). Commentary on the evolution of transmitters, receptors and ion channels in invertebrates. Comparative Biochemistry and Physiology 93A, 2539.CrossRefGoogle ScholarPubMed
Williams, H. H., McVicar, A. H. & Ralph, R. (1970). The alimentary canal of fish as an environment for helminth parasites. Symposium of the British Society for Parasitology 8, 4377.Google Scholar