Abstract
Using an indirect immunofluorescence technique interfaced with confocal scanning laser microscopy, whole-mount preparations of three general of marine trematode larvae,Cryptocotyle lingua, Cercaria emasculans andHimasthla leptosoma, were screened for 5-hydroxytryptamine (5-HT) and selected neuropeptide immunoreactivities (IRs). IRs for pancreatic polypeptide (PP), peptide YY (PYY) and FMRFamide were found in the central nervous systems of the three species of cercariae, immunostaining the paired ganglia and central commissure and the longitudinal nerve cords, with slight differences in both distribution and intensity of IRs being observed for the different antisera used. PP, PYY and FMRFamide IRs were evident in both central and peripheral components of the nervous system in the rediae ofC. lingua. 5-HT IR was confined to the peripheral nervous systems of the cercariae ofC. emasculans and the rediae ofC. lingua, appearing in the form of a network of immunoreactive fibres and associated large cell bodies. A moderate substance P IR was observed in the nervous system of the cercariae ofC. lingua. The patterns of immunostaining described were compared with those obtained using antiserum directed to the C-terminal decapeptide amide of neuropeptide F (NPF), a native parasitic peptide from the cestodeMoniezia expansa. Results demonstrated that serotoninergic and peptidergic components were present in the nervous systems of all of the trematode larvae studied and that some, if not all, of the IR for PP, PYY and FMRFamide was due to the presence of a trematode NPF homologue.
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References
Barton CL, Halton DW, Shaw C, Maule AG, Johnston CF (1993) An immunocytochemical study of putative neurotransmitters in the metacercariae of two strigeoid trematodes from rainbow trout (Oncorhynchus mykiss). Parasitol Res 79:389–396
Bennett JL, Gianutsos G (1977) Distribution of catecholamines in immatureFasciola hepatica: a histochemical and biochemical study. Int J Parasitol 7:221–225
Boer HH, Schot LPC, Veenstra JA, Reichelt D (1980) Cytochemical identification of neural elements in the central nervous systems of the snail, some insects, a fish, and a mammal with antiserum to the molluscan cardio-excitatory tetrapeptides FMRFamide. Cell Tissue Res 213:21–27
Chen ST, Tsai MS, Shen CL (1989) Distribution of FMRFamidelike immunoreactivity in the central nervous system of the Formosan monkey (Macaca cyclopsis). Peptides 20:825–834
Cottrell GA (1989) The biology of the FMRF-amide series of peptides in molluscs with special reference toHelix. Comp Biochem Physiol [A] 93:41–45
Cowden C, Stretton AOW, Davis PF (1989) AF1, a sequenced bioactive neuropeptide isolated from the nematodeAscaris suum. Neuron 2:1465–1473
Dei-Cas E, Dhainaut-Courtois N, Dhainaut A, Vernes A (1979) Ultrastructural localization of tritiated 5-HT in adultSchistosoma mansoni, preliminary report. Biol Cell 35:321–324
Fairweather I, Halton DW (1991) Neuropeptides in platyhelminths. Parasitology 102:S77-S92
Fairweather I, Mahendrasingam S, Johnston CF, Halton DW, Shaw C (1990) Peptidergic nerve elements in three developmental stages of the tetraphyllidean tapewormTrilocularia acanthiaevulgaris. Parasitol Res 76:497–508
Geary TG, Price DA, Bowman JW, Winterrowd CA, Mackenzie CD, Garrison RD, Williams JF, Friedman AR (1992) Two FMRFamide-like peptides from the free-living nematodePanagrellus redivivus. Peptides 13:209–214
Grimmelikhuijzen CJP (1986) FMRFamide-like peptides in the primitive nervous systems of higher animals. In: Stefano GB (ed) Handbook of comparative opioid and related neuropeptide mechanisms, vol 1. CRC, Boca Raton, Florida, pp 103–115
Gustafsson MKS (1988) The helminth nervous system. In: Mehlhorn H (ed) Parasitology in focus. Facts and trends. Springer, Berlin Heidelberg New York London Paris Tokyo, pp 295–310
Gustafsson MKS (1992) The neuroanatomy of parasitic flatworms. Adv Neuroimmunol 2:267–286
Gustafsson MKS, Wikgren MC, Karhi TJ, Schot LPC (1985) Immunocytochemical demonstration of neuropeptides and serotonin in the tapewormDiphyllobothrium dendriticum. Cell Tissue Res 240:255–260
Halton DW, Fairweather I, Shaw C, Johnston CF (1990) Regulatory peptides in parasitic platyhelminths. Parasitol Today 6: 284–290
Halton DW, Shaw C, Maule AG, Johnston CF, Fairweather I (1992) Peptidergic messengers: a new perspective of the nervous system of parasitic platyhelminths. J Parasitol 78: 179–193
Mansour TE (1984) Serotonin receptors in parasitic worms. Adv Parasitol 23:1–36
Maule AG, Halton DW, Allen JM, Fairweather I (1989) Studies on motility in vitro of an ectoparasitic monogenean,Diclidophora merlangi. Parasitology 98:85–93
Maule AG, Shaw C, Halton DW, Thim L, Johnston CF, Fairweather I (1991) Neuropeptide F: a novel parasitic flatworm regulatory peptide fromMoniezia expansa (Cestoda: Cyclophyllidea). Parasitology 102:309–316
McKay DM, Halton DW, Johnston CF, Fairweather I, Shaw C (1990) Occurrence and distribution of putative neurotransmitters in the frog lung parasiteHaplometra cylindracea (Trematoda: Digenea). Parasitol Res 76:509–517
Niewiadomska K, Maslinska D, Czubaj A, Pomorski P (1993) Distribution of serotonin immunoreactive (5HT-IR) neurons and fibres in metacercaria ofDiplostomum paracaudum (Iles, 1959) (Digenea). Acta Parasitol 38:52–54
Painter SD (1982) FMRFamide catch contractures of a molluscan smooth muscle: pharmacology, ionic dependence and cyclic nucleotides. J Comp Physiol 148:491–501
Skuce PJ, Johnston CF, Fairweather I, Halton DW, Shaw C (1990a) A confocal scanning laser microscope study of the peptidergic and serotoninergic components of the nervous system in larvalSchistosoma mansoni. Parasitology 101:227–234
Skuce PJ, Johnston CF, Fairweather I, Halton DW, Shaw C (1990b) Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke,Schistosoma mansoni. Cell Tissue Res 261:573–581
Stretton AOW, Cowden C, Sithigorngul P, Davis RE (1991) Neuropeptides in the nematodeAscaris suum. Parasitology 102:S107-S116
Tomosky-Sykes TK, Jardine I, Mueller JF, Bueding E (1977) Source of error in neurotransmitter analysis. Anal Biochem 83:99–108
Walker RJ, Holden-Dye L (1989) Commentary on the evolution of transmitters, receptors and ion channels in invertebrates. Comp Biochem Physiol [A] 93:25–39
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Pan, J.Z., Halton, D.W., Shaw, C. et al. Serotonin and neuropeptide immunoreactivities in the intramolluscan stages of three marine trematode parasites. Parasitol Res 80, 388–395 (1994). https://doi.org/10.1007/BF00932376
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DOI: https://doi.org/10.1007/BF00932376