Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T12:00:49.320Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunocytochemical and radioimmunometrical demonstration of serotonin- and neuropeptide-immunoreactivities in the adult rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophyllidea)

Published online by Cambridge University Press:  06 April 2009

D. M. McKay ,
I. Fairweather ,
C. F. Johnston ,
C. Shaw  and
D. W. Halton
D. M. McKay
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, The Queen's University, Belfast BT7 1NN, Northern, Ireland
I. Fairweather
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, The Queen's University, Belfast BT7 1NN, Northern, Ireland
C. F. Johnston
Affiliation:
Comparative Neuroendocrinology Research Group, Department of Medicine, The Queen's University, Belfast BT7 1NN, Northern, Ireland
C. Shaw
Affiliation:
Comparative Neuroendocrinology Research Group, Department of Medicine, The Queen's University, Belfast BT7 1NN, Northern, Ireland
D. W. Halton
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, The Queen's University, Belfast BT7 1NN, Northern, Ireland
Get access Rights & Permissions [Opens in a new window]

Abstract

Standard indirect immunocytochemical techniques have been interfaced with confocal scanning laser microscopy (for whole-mount preparations) and epifluorescence microscopy (for cryosections) to investigate the occurrence and distribution of serotoninergic and peptidergic nerve elements in adult H. diminuta. Serotonin (5-HT)-immunoreactivity (IR) was widespread throughout the worm, occurring in the paired cerebral ganglia, transverse commissure, the 10 longitudinal nerve cords and in a plethora of small nerve fibres of the peripheral nervous system. An abundance of serotoninergic nerve cell bodies was found in association with the lateral nerve cords. The genital atrium and accessory reproductive ducts were richly innervated with serotoninergic nerve fibres. Thirty-five antisera to 20 vertebrate regulatory peptides and 1 invertebrate peptide (FMRFamide) were used to screen the worm for neuropeptide IR. Immunostaining was obtained with antisera raised to pancreatic polypeptide (PP), peptide YY (PYY), neuropeptide Y (NPY), substance P (SP), peptide histidine isoleucine (PHI), xenopsin (XP) and FMRFamide. The most extensive pattern of IR occurred with antisera to PP and PYY, IR being evident in the cerebral ganglia, transverse commissure, longitudinal nerve cords and in small nerve fibres that ramified throughout the parenchyma. A series of bipolar nerve cell bodies between the median nerve cords displayed PP/PYY-IR. The distribution of FMRFamide-IR was reminiscent of the PP/PYY pattern but was less extensive. Comparison of the serotoninergic and peptidergic nervous systems has revealed general similarities and some distinct differences, especially with regard to the distribution of immunoreactive nerve cell bodies. Quantitative data are presented on the levels of PP-, SP-, PH1-, and gastrin-releasing peptide (GRP)-immunoreactivities demonstrable in acid-alcohol extracts of whole worms. The highest level of peptide IR determined was recorded for PP.

Keywords

Hymenolepis diminutaCestodaCyclophyllideaserotonin (5-hydroxytryptamine)neuropeptidesimmuno-cytochemistryconfocal microscopyradioimmunoassay
Type
Research Article
Information
Parasitology , Volume 103 , Issue 2 , October 1991 , pp. 275 - 289
Copyright
Copyright © Cambridge University Press 1991

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.)

References

Araki, K., Tachibana, S., Uchiyama, M., Nakajima, T. & Yasuhara, T. (1973). Isolation and structure of a new peptide ‘xenopsin’ on the smooth muscle, especially on a strip of fundus from a rat stomach, from the skin of Xenopus laevis. Chemical Pharmaceutical Bulletin 21, 2801–4.CrossRefGoogle ScholarPubMed
Armstrong, P. E., Foy, W. L., Johnston, C. F., Shaw, C., Murphy, R. F. & Buchanan, K. D. (1989). Peptide histidine isoleucine (PHI) immunoreactivity in the rat retina: identification and characterisation by radioimmunoassay, immunohistochemistry and high-performance liquid chromatography. Regulatory Peptides 25, 325–32.CrossRefGoogle ScholarPubMed
Bateson, P. G., Buchanan, K. D., Stewart, D. M. & Parks, T. G. (1980). The release of vasoactive intestinal peptide during altered mid-gut blood flow. British Journal of Surgery 67, 131–4.CrossRefGoogle ScholarPubMed
Carraway, R. E. & Reinecke, M. (1989). Neurotensin and related peptides. In ‘The Comparative Physiology of Regulatory Peptides’ (ed. Holmgren, S.), pp. 87–111. London: Chapman and Hall Ltd.CrossRefGoogle 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 Scholar
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.CrossRefGoogle ScholarPubMed
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
Eklove, H. & Webb, R. A. (1990). Glutamate-like immunoreactivity in the cestode Hymenolepis diminuta. Canadian Journal of Zoology 68, 2417–23.CrossRefGoogle Scholar
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in parasitic platyhelminths. Parasitology 102, S77–S92.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 74, 371–9.CrossRefGoogle ScholarPubMed
Fairweather, I., Mahendrasingham, S., Johnston, C. F., Halton, D. W., McCullough, J. S. & Shaw, C. (1990 a). An ontogenetic study of the cholinergic and serotoninergic nervous systems in Trilocularia acanthiaevulgaris (Cestoda, Tetraphyllidea). Parasitology Research 76, 487–96.CrossRefGoogle ScholarPubMed
Fairweather, I., Mahendrasingham, S., Johnston, C. F., Halton, D. W. & Shaw, C. (1990 b). Peptidergic nerve elements in three developmental stages of the tetraphyllidean tapeworm Trilocularia acanthiaevulgaris. An immunocytochemical study. Parasitology Research 76, 497–508.CrossRefGoogle ScholarPubMed
Greenberg, M. J., Payza, K., Nachman, R. J., Holman, G. M. & Price, D. A. (1988). Relationships between the FMRFamide-related peptides and other peptide families. Peptides 9, Suppl. 1, 125–35.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Lehtonen, M. A. I. & Sundler, F. (1986). Immunocytochemical evidence for the presence of ‘mammalian’ neurohormonal peptides in neurones of the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 243, 41–9.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Wikgren, M. C., Karhi, T. J. & Schot, L. P. C. (1985). Immunocytochemical demonstration of neuropeptides and serotonin in the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 240, 255–60.CrossRefGoogle ScholarPubMed
Halton, D. W., Fairweather, I., Shaw, C. & Johnston, C. F. (1990). Regulatory peptides in parasitic platyhelmiths. Parasitology Today 6, 284–90.CrossRefGoogle Scholar
Hariri, M. (1974 a). Quantitative measurements of endogenous levels of acetylcholine and choline in tetrathyridia of Mesocestoides corti (Cestoda) by means of combined gas chromatograph-mass spectrometry. Journal of Parasitology 60, 227–30.CrossRefGoogle Scholar
Hariri, M. (1974 b). Occurrence and concentration of biogenic amines in Mesocestoides corti (Cestoda). Journal of Parasitology 60, 737–43.CrossRefGoogle ScholarPubMed
Kaloustian, K. V. & Edmands, J. A. (1986). Immunocytochemical 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 Scholar
Kuhlman, J. R., Li, C. & Calabrese, R. L. (1985). FMRFamide-like substances in the leech. II. Bioactivity on the heartbeat system. Journal of Neuroscience 5, 2310–17.CrossRefGoogle Scholar
Kumazawa, H. & Moriki, T. (1986). Immunoenzymatic demonstration of a presumptive prolactin-like substance in Hymenolepis nana. Zeitschrift für Parasitenkunde 72, 137–9.CrossRefGoogle ScholarPubMed
Li, C. & Calabrese, R. L. (1987). FMRFamide-like substances in the leech. III. Biochemical characterization and physiological effects. Journal of Neuroscience 7, 595–603.CrossRefGoogle ScholarPubMed
Lumsden, R. D. & Specian, R. (1980). The morphology, histology, and fine structure of the adult stage of the cyclophyllidean tapeworm Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H. P.), pp. 157–280. New York and London: Academic Press.CrossRefGoogle Scholar
McFarlane, I. D., Graff, D. & Grimmelikhuijzen, C. J. P. (1987). Excitatory actions of Antho-RFamide, an anthozoan neuropeptide, on muscles and conducting systems in the sea anemone Calliactis parasitica. Journal of Experimental Biology 133, 157–68.CrossRefGoogle Scholar
McKay, D. M., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1990 a). 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 b). 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 Scholar
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
Magee, R. M., Fairweather, I., Shaw, C., McKillop, J. M., Montgomery, W. I., Johnston, C. F. & Halton, D. W. (1991 a). Quantification and partial characterisation of regulatory peptides in the liver fluke, Fasciola hepatica from different mammalian hosts. Comparative Biochemistry and Physiology 99C, 201–7.Google Scholar
Magee, R. M., Shaw, C., Fairweather, I., Thim, L., Johnston, C. F. & Halton, D. W. (1991 b). Isolation and partial sequencing of a pancreatic polypeptide-like neuropeptide from the liver fluke, Fasciola hepatica. Comparative Biochemistry and Physiology (in the Press).Google ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F. & Fairweather, I. (1989 a). 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., Shaw, C., Halton, D. W., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1989 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., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255–73.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
McKillop, J. M., Foy, W. L., Johnston, C. F., Shaw, C., Murphy, R. F. & Buchanan, K. D. (1988). Gastrin-releasing peptide (GRP) in the rat retina: a radioimmunoassay, immunohistochemical and chromatographic study. Brain Research 447, 239–45.CrossRefGoogle ScholarPubMed
O'Hare, M. M. T., Daly, J. G. & Buchanan, K. D. (1983). Radioimmunoassay for pancreatic polypeptide, and its age-related changes in concentration. Clinical Chemistry 29, 1923–7.CrossRefGoogle ScholarPubMed
Phillis, J. W. (1970). The Pharmacology of Synapses. Oxford: Pergamon Press.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 Scholar
Rahman, M. S., Mettrick, D. F. & Podesta, R. B. (1983). Effects of 5-hydroxytryptamine on carbohydrate metabolism in Hymenolepis diminuta (Cestoda). Canadian Journal of Physiology and Pharmacology 61, 137–43.CrossRefGoogle ScholarPubMed
Ribeiro, P. & Webb, R. A. (1983). The occurrence and synthesis of octopamine and catecholamines in the cestode Hymenolepis diminuta. Molecular and Biochemical Parasitology 7, 53–62.CrossRefGoogle ScholarPubMed
Ribeiro, P. & Webb, R. A. (1984). The occurrence, synthesis and metabolism of 5-hydroxytryptamine and 5-hydroxytrptophan in the cestode Hymenolepis diminuta: a high performance liquid chromatographic study. Comparative Biochemistry and Physiology 79C, 159–64.Google Scholar
SalÓ, E. & BaguÑÀ, J. (1986). Stimulation of cellular proliferation and differentiation in the intact and regenerating planarian Dugesia (G) tigrina by the neuropeptide substance P. Journal of Experimental Zoology 237, 129–35.CrossRefGoogle ScholarPubMed
Samii, S. I. & Webb, R. A. (1990). Acetylcholine-like immunoreactivity in the cestode Hymenolepis diminuta. Brain Research 513, 161–5.CrossRefGoogle ScholarPubMed
Shaw, C., Thim, L. & Conlon, J. M. (1986). [Ser7] neurotensin: isolation from guinea pig intestine. FEBS Letters 202, 187–92.CrossRefGoogle ScholarPubMed
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
Sukhdeo, M. V. K., Hsu, S. C., Thompson, C. S. & Mettrick, D. F. (1984). Hymenolepis diminuta: behavioral effects of 5-hydroxytryptamine, acetylcholine, histamine and somatostatin. Journal of Parasitology 70, 682–8.CrossRefGoogle ScholarPubMed
Thompson, C. S., Sangster, N. C. & Mettrick, D. F. (1986). Cholinergic inhibition of muscular contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 64, 2111–15.CrossRefGoogle Scholar
Thompson, C. S. & Mettrick, D. F. (1989). The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 1257–62.CrossRefGoogle Scholar
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. and Van Noorden, S.), pp. 308–27. Bristol: John Wright and Sons Ltd.Google Scholar
Webb, R. A. (1985). The uptake and metabolism of 5-hydroxytryptamine by tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 80C, 305–12.Google Scholar
Webb, R. A. (1986). The uptake and metabolism of L-glutamate by tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 85C, 151–62.Google Scholar
Webb, R. A. & Eklove, H. (1989). Demonstration of intense glutamate-like immunoreactivity in the longitudinal nerve cords of the cestode Hymenolepis diminuta. Parasitology Research 75, 545–8.CrossRefGoogle ScholarPubMed
Webb, R. A. & Mizukawa, K. (1985). Serotonin like immunoreactivity in the cestode Hymenolepis diminuta. Journal of Comparative Neurology 234, 431–40.CrossRefGoogle Scholar
Wikgren, M., Reuter, M. & Gustafsson, M. (1986). Neuropeptides in free-living and parasitic flatworms (Platyhelminthes). An immunocytochemical study. Hydrobiologia 132, 93–9.CrossRefGoogle Scholar
Wilson, V. C. L. C. & Schiller, E. L. (1969). The neuroanatomy of Hymenolepis diminuta and H. nana. Journal of Parasitology 55, 261–70.CrossRefGoogle ScholarPubMed