Abstract
Whole mounts of the metacercariae ofDiplostomum sp. andCotylurus erraticus from rainbow trout have been treated cytochemically for the demonstration of cholinergic, serotoninergic (5-hydroxytryptamine) and peptidergic elements in the nervous system. Antisera directed against four vertebrate (pancreatic polypeptide, peptide YY, substance P and peptide histidine isoleucine) and two invertebrate peptides (neuropeptide F and FMR Famide) were used in an indirect immunofluorescence procedure in conjunction with confocal scanning laser microscopy (CSLM). Of the seven antisera tested, all except peptide histidine isoleucine showed significant immunoreactivity. Cholinergic and serotoninergic staining was found primarily in the central nervous system (CNS) and in cell bodies associated with the ventral and dorsal nerve cords in both trematodes. Peptidergic immunoreactivity was localised in the CNS and PNS of both genera, revealing an extensive innervation within the holdfast organ and in and around the oral and ventral suckers.
Similar content being viewed by others
References
Barton CL, Shaw C, Halton DW, Johnston CF, Buchanan KD (1992) Distribution and characterisation of neuropeptide Y immunoreactivity in the brain and gastrointestinal tract of the rainbow trout,Oncorhynchus mykiss. Comp Biochem Physiol 103C:175–180
Betterton C (1974) Studies on the host specificity of the eyeflukeDiplostomum spathaceum in brown and rainbow trout. Parasitology 69:11–29
Bortz BM, Kenny GE, Pauley GB, Garcia-Ortigoza E, Anderson DP (1984) The immune response in immunised and naturally infected rainbow trout (Salmo gairdneri) toDiplostomum spathaceum as detected by ELISA. Dev Comp Immunol 8:813–822
Chubb JC (1979) Seasonal occurrence of helminths in freshwater fishes. Adv Parasitol 17:141–313
Coons AH, Lebuc EH, Connolly JM (1955) Studies on antibody production: I. A method for the histochemical demonstration of specific antibodies and its application to a study of the hyperimmune rabbit. J Exp Med 102:49–60
De Loof A, Schoofs L (1990) Homologies between the amino acid sequences of some vertebrate peptide hormones and peptides isolated from invertebrate sources. Comp Biochem Physiol [B] 95:459–468
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 tapeworm,Trilocularia acanthiaevulgaris: an immunocytochemical study. Parasitol Res 74:371–379
Gomori G (1952) Microscopic histochemistry, ch 8. University of Chicago Press, Chicago, pp 137–221
Gustafsson MKS (1988) Helminth nervous system. In: Mehlhorn H (ed) Parasitology in focus, ch 3. Springer, Berlin Heidelberg New York, pp 295–310
Halton DW (1968) Light and electron microscope studies of carboxylic esterase activity in the trematodeHaplometra cylindracea. J Parasitol 54:1124–1130
Halton DW, Fairweather I, Shaw C, Johnston CF (1990) Regulatory peptides in parasitic platyhelminths. Parasitol Today 6:284–290
Halton DW, Brennan GP, Maule AG, Shaw C, Johnston CF, Fairweather I (1991) The ultrastructure and immunogold labelling of pancreatic polypeptide-immunoreactive cells associated with the egg-forming apparatus of a monogenean parasite,Diclidophora merlangi. Parasitology 102:429–436
Halton DW, Shaw C, Maule AG, Johnston CF, Fairweather I (1992) Peptidergic messengers: a new perspective of the nervous system of parasitic plathelminths. J Parasitol 78:179–193
Hillman GR (1983) The neuropharmacology of schistosomes. Pharmacol Ther 22:103–115
Holmes SD, Fairweather I (1984)Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Exp Parasitol 58:194–208
Holmgren S, Vaillant C, Dimaline R (1982) VIP-, substance P, gastrin/CCK-, bombesin-, somatostatin- and glucagon-like immunoreactivities in the gut of the rainbow trout,Salmo gairdneri. Cell Tissue Res 223:141–153
Magee RM, Fairweather I, Johnston CF, Halton DW, Shaw C (1989) Immunocytochemical demonstration of neuropeptides in the nervous system of the liver fluke,Fasciola hepatica (Trematoda, Digenea). Parasitology 98:227–238
Magee RM, Fairweather I, Shaw C, McKillop JM, Montgomery WI, Johnston CF, Halton DW (1991) Quantification and partial characterisation of regulatory peptides in the liver flukeFasciola hepatica from different mammalian hosts. Comp Biochem Physiol [B] 99:201–207
Mansour TE (1984) Serotonin receptors in parasitic worms. Adv Parasitol 23:1–36
Maule AG, Halton DW, Allen JM, Fairweather I (1989a) Studies of the motility in vitro of the ectoparasitic monogenean,Diclidophora merlangi. Parasitology 98:85–93
Maule AG, Halton DW, Johnston CF, Fairweather I, Shaw C (1989b) Immunocytochemical demonstration of neuropeptides in the fish-gill parasite,Diclidophora merlangi (monogenoidea). Int J Parasitol 19:307–316
Maule AG, Shaw C, Halton DW, Johnston CF, Fairweather I, Buchanan KD (1989c) Tachykinin immunoreactivity in the parasitic flatwormDiclidophora merlangi and its fish host the whiting (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera. Comp Biochem Physiol [B] 94:533–541
Maule AG, Halton DW, Johnston CF, Shaw C, Fairweather I (1990a) A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system in the monogenean parasite,Diclidophora merlangi. Parasitol Res 76:409–419
Maule AG, Halton DW, Johnston CF, Fairweather I (1990b) The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite,Diclidophora merlangi: a cytochemical study. Parasitology 100:255–273
Maule AG, Shaw C, Halton DW, Thim L, Johnston CF, Fairweather I, Buchanan KD (1992) Neuropeptide F: a novel parasitic flatworm regulatory peptide fromMoniezia expansa (Cestodea: Cyclophyllidea). Parasitology 102:309–316
McKay DM, Halton DW, Allen JM, Fairweather I (1989) The effects of cholinergic and serotoninergic drugs on motility in vitro ofHaplometra cylindracea (Trematoda: Digenea). Parasitology 99:241–252
McKay DW, Shaw C, Halton DW, Johnston CF, Fairweather I, Buchanan KD (1990) Mammalian regulatory peptide immunoreactivity in the trematode parasiteHaplometra cylindracea and the lung of its frog host,Rana temporaria: comparative chromatographic characterisation using reverse phase high performance chromatography. Comp Biochem Physiol [B] 96:345–351
McKay DW, Halton DW, Johnston CF, Fairweather I, Shaw C (1991) Cytochemical demonstration of cholinergic, serotoninergic and peptidergic nerve elements inGorgoderina vitelliloba (Trematoda: Digenea). Int J Parasitol 21:71–80
Mitchell JS (1981) Observations on the development in vitro ofCotylurus erraticus (Trematoda: strigeidae) from the metacercaria to the patent adult. PhD Thesis, The Queen's University of Belfast
Niewiadomska N, Moczon T (1982) The nervous system ofDiplostomum pseudospathaceum Niewiadomska (Digenea, Diplostomatidae): I. Nervous system and chactotaxy in cercaria. Z Parasitenkd 68:295–304
Niewiadomska K, Moczon T (1984) The nervous system ofDiplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomatidae): II. Structure and development of the nervous system in metacercaria. Z Parasitenkd 70:537–548
Niewiadomska N, Moczon T (1987) The nervous system ofDiplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomatidae): III. Structure of the nervous system in the adult stage. Parasitol Res 73:46–49
Olsen RE (1978) Parasites of silver (coho) salmon and king (chinook) salmon from the Pacific ocean off Oregon. Calif Fish Game 64:117–120
Platt N, Reynolds SE (1988) Invertebrate neuropeptides. In: Lunt GG, Olsen RW (eds) Comparative invertebrate neurochemistry. Croom Helm Ltd, Beckenham, pp 175–226
Reuter M (1987) Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system ofGyrodactylus solaris (Monogeanea). Acta Zool 68:187–193
Rushton W (1937) Blindness in freshwater fish. Nature 140:1014
Shariff M, Richards RH, Sommerville C (1980) The histopathology of acute and chronic infections of rainbow troutSalmo gairdneri Richardson with eye flukes,Diplostomum spp. J Fish Dis 3:455–465
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, Buchanan KD (1990b) Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood flukeSchistosoma mansoni. Cell Tissue Res 261:573–581
Speed P, Pauley GB (1985) Feasibility of protecting rainbow trout,Salmo gairdneri, Richardson, by immunity against the eye fluke,Diplostomum spathaceum. J Fish Biol 26:739–744
Stables JN, Chappell LH (1986a)Diplostomum spathaceum (Rud. 1819): effects of physical factors on the infection of rainbow trout (Salmo gairdneri) by cercariae. Parasitology 93:71–79
Stables JN, Chappell LH (1986b) Putative immune response of the rainbow trout,Salmo gairdneri, toDiplostomum spathaceum infection. J Fish Biol 29:115–122
Sweeting RA (1974) Investigations into the natural and experimental infections of freshwater fish by the common eye-flukeDiplostomum spathaceum Rud. Parasitology 69:291–300
Walker RJ (1992) Neuroactive peptides with an RFamide or Famide carboxyl terminal. Comp Biochem Physiol [B] 102:213–222
Whyte SK, Allan JC, Secombes CJ, Chappell LH (1986) Cercariae and diplostomules ofDiplostomum spathaceum (Digenea) elicit an immune response in rainbow trout,Salmo gairdneri, Richardson. J Fish Biol 31 [Suppl A]:185–190
Whyte SK, Chappell LH, Secombes CJ (1988) In vitro transformation ofDiplostomum spathaceum (Digenea) cercariae and short term maintenance of post-penetration larvae in vitro. J Helminthol 62:293–302
Whyte SK, Chappell LH, Secombes CJ (1989) Cytotoxic reactions of rainbow trout,Salmo gairdneri Richardson, macrophages for larvae of the eye flukeDiplostomum spathaceum (Digenea). J Fish Biol 35:333–345
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Barton, C.L., Halton, D.W., Shaw, C. et al. An immunocytochemical study of putative neurotransmitters in the metacercariae of two strigeoid trematodes from rainbow trout (Oncorhynchus mykiss). Parasitol Res 79, 389–396 (1993). https://doi.org/10.1007/BF00931828
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00931828