Abstract
The reproductive system of the monogenean gill parasite,Diclidophora merlangi, was examined for the presence of cholinergic, serotoninergic and peptidergic innervation using cytochemical and immunocytochemical techniques. Cholinesterase activity and 5-hydroxytryptamine immunoreactivity (5-HT-IR) were confined to neural elements of the male reproductive system, being evident in the innervation of the cirrus, whereas only 5-HT was present in nerves and somata of the elongate seminal vesicle. Peptidergic innervation was localised to both the male and female reproductive systems of the worm. Within the female reproductive apparatus pancreatic polypeptide, peptide tyrosine tyrosine, neuropeptide Y, substance P, neurokinin A, eledoisin, FMRFamide and gastrin/cholecystokinin immunoreactive fibres and somata were observed in the oviduct, vitelline reservoir and ovovitelline duct. Intense peptide immunoreactivity was identified in fibres in the wall of the ootype and in a surrounding population (>100) of somata that were situated beyond Mehlis' gland cells and all of which were connected to the ootype wall by fine cytoplasmic connectives. The strategic location of this peptidergic cell population infers its involvement in the egg-forming sequence in this platyhelminth parasite.
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Baguñà J, Ballester R (1978) The nervous system in planarians: peripheral and gastrodermal plexuses, pharynx innervation, and the relationship between central nervous system structure and the acoelomate organization. J Morphol 155: 237–252
Basch PF, Gupta BC (1988) Immunocytochemical localization of regulatory peptides in six species of trematode parasites. Comp Biochem Physiol [C] 91: 565–570
Bautz A, Schilt J, Richoux J-P, Dubois M-P (1980) Detection immunocytologique, denombrement et localisation des cellules a somatostatine (SRIF) chez deux especes de Planaires,Dugesia lugubris etDendrocoelum lacteum (Turbellaries, Triclades). C R Seances Acad Sci 291: 833–836
Beauvillain JC, Tramu G, Garaud J (1984) Coexistence of substances related to enkephalin and somatostatin in granules of the guinea-pig median eminence: demonstration by use of colloidal gold immunocytochemical methods. Brain Res 301: 389–393
Carraway R, Ruane SE, Kim H-R (1982) Distribution and immunochemical character of neurotensin-like material in representative vertebrates and invertebrates: apparent conservation of the COOH-terminal region during evolution. Peptides 1: 115–123
Coons AH, Leduc EH, Connolly JM (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. J Exp Med 102: 49–60
Dockray GJ, Williams RG (1983) FMRFamide-like immunoreactivity in rat brain: development of a radioimmunoassay and its application in studies of distribution and chromatographic properties. Brain Res 266: 295–303
Dockray GJ, Vaillant C, Williams RG (1981) New vertebrate braingut peptide related to a molluscan neuropeptide and an opioid peptide. Nature 293: 656–657
Evans BD, Calabrese RL (1989) Small cardioactive peptide-like immunoreactivity and its colocalization with FMRFamide-like immunoreactivity in the central nervous system of the leechHirudo medicinalis. Cell Tissue Res 257: 187–199
Fairweather I, Maule AG, Mitchell SH, Johnston CF, Halton DW (1987) Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) in the nervous system of the liver fluke,Fasciola hepatica (Trematoda, Digenea). Parasitol Res 73: 255–258
Fairweather I, Macartney GA, Johnston CF Halton DW Buchanan KD (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). Parasitol Res 74: 371–379
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 (in press)
Fetterer RH, Pax RA, Bennett JL (1977)Schistosoma mansoni: direct method for simultaneous recording of electrical and motor activity. Exp Parasitol 43: 286–294
Frankland HMT (1955) The life history and bionomics ofDiclidophora denticulata (Trematoda, Monogenea). Parasitology 45: 313–351
Gomori G (1952) Microscopic histochemistry, principles and practice. University of Chicago Press, Chicago
Greenberg MJ, Price DA (1983) Invertebrate neuropeptides: native and naturalized. Ann Rev Physiol 45: 271–288
Grimmelikhuijzen CJP (1983) Coexistence of neuropeptides in hydra. Neuroscience 9: 837–845
Gupta BC, Basch PF (1989) Human chorionic gonadotropin-like immunoreactivity in schistosomes andFasciola. Parasitol Res 76: 86–89
Gustafsson MKS (1985) Cestode neurotransmitters. Parasitol Today 1: 72–75
Gustafsson MKS (1987) Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adultSchistosoma mansoni. Parasitol Res 74: 168–174
Gustafsson MKS, Wikgren MC (1989) Development of immunoreactivity to the invertebrate neuropeptide small cardiac peptide B in the tapewormDiphyllobothrium dendriticum. Parasitol Res 75: 396–400
Gustafsson MKS, Wikrgren MC, Karhi TJ, Schot LPC (1985) Immunocytochemical demonstration of neuropeptides and serotonin in the tapewormDiphyllobothrium dendriticum. Cell Tissue Res 240: 255–260
Gustafsson MKS, Lehtonen MAI, Sundler F (1986) Immunocytochemical evidence for the presence of “mammalian” neurohormonal peptides in neurones of the tapewormDiphyllobothrium dendriticum. Cell Tissue Res 243: 41–49
Halton DW, Arme C (1971) An in vitro technique for detecting tissue damage inDiclidophora merlangi: possible screening method for selection of undamaged tissues or organisms prior to physiological investigation. Exp Parasitol 30: 54–57
Halton DW, Morris GP (1969) Occurrence of cholinesterase and ciliated sensory structures in a fish gill fluke,Diclidophora merlangi (Trematoda, Monogenea). Z Parasitenkd 33: 21–30
Halton DW, Maule AG, Johnston CF, Fairweather I (1987) Occurrence of 5-hydroxytryptamine (serotonin) in the nervous system of a monogenean,Diclidophora merlangi Parasitol Res 74: 151–154
Hardcastle A (1977) Ultrastructural observations on the reproductive system ofDiclidophora merlangi (Monogenoidea: Polyopisthocotylea). PhD Thesis, The Queen's University of Belfast, Northern Ireland
Haynes LW (1980) Peptide neuroregulators in invertebrates. Prog Neurobiol 15: 205–245
Hökfelt T, Holets VR, Staines W, Meister B, Melander T, Schalling M, Schutlzberg M, Freedman J, Björklund H, Olson L, Lindh B, Elfvin L-G, Lundberg JM, Lindgren JA, Samuelsson B, Pernow B, Terenius L, Post C, Everitt B, Goldstein M, (1986) Coexistence of neuronal messengers—an overview. Prog Brain Res 68: 33–70
Hökfelt T, Millhorn D, Seroogy K, Tsuruo Y, Ceccatelli S, Lindh B, Meister B, Melander T, Schalling M, Bartfai T, Terenius L (1987) Coexistence of peptides with classical neurotransmitters. Experientia 43: 768–780
Holmes SD, Fairweather I (1984)Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Exp Parasitol 58: 194–208
Jennings JB, Davenport TRB, Varndell IM (1987) FMRFamide-like immunoreactivity and arylamidase activity in turbellarians and nemerteans—evidence for a novel neurovascular coordinating system in nemerteans. Comp Biochem Physiol [C] 86: 425–430
Kearn GC (1986) The eggs of monogeneans. Adv Parasitol 25: 175–273
Koelle GB, (1951) Elimination of enzymatic diffusion artifacts in histochemical localization of cholinesterase and survey of their cellular distribution. J Pharm Exp Ther 103: 153–171
Kumazawa H, Moriki T (1986) Immunoenzymatic demonstration of a presumptive prolactin-like substance inHymenolepis nana. Z Parasitenkd 72: 137–139
Le Roith D, Shiloach J, Roth J (1982) Is there an earlier phylogenetic precursor that is common to both the nervous and endocrine systems? Peptides 3: 211–215
Le Roith D, Shiloach J, Berelowitz M, Frohman LA, Liotta AS, Krieger DT, Roth J (1983) Are messenger molecules in microbes the ancestors of the vertebrate hormones and tissue factors? Fed Proc 42: 2602–2607
Löser E (1965) Der Feinbau des Oogenotop bei Cestoden. Z Parasitenkd 25: 413–458
Lundberg JM Hökfelt T (1983) Coexistence of peptides and classical neurotransmitters. Trends Neuropharmacol Sci 6: 325–333
Macdonald S, Caley J (1975) Sexual reproduction in the monogeneanDiclidophora merlangi: tissue penetration by sperms. Z Parasitenkd 45: 323–334
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
Mansour TE (1984) Serotonin receptors in parasitic worms. Adv Parasitol 23: 1–36
Maule AG, Halton DW, Johnston CF, Fairweather I, Shaw C (1989a) Immunocytochemical demonstration of neuropeptides in the fish-gill parasite,Diclidophora merlangi (Monogenoidea). Int J Parasitol 19: 307–316
Maule AG, Halton DW, Johnston CF, Shaw C, Fairweather I (1989b) The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite,Diclidophora merlangi: a cytochemical study. Parasitology (in press)
Maule AG, Halton DW, Allen JM, Fairweather I (1989c) Studies on motility in vitro of an ectoparasitic monogenean,Diclidophora merlangi. Parasitology 98:85–93
Maule AG, Shaw C, Halton DW, Johnston CF, Fairweather I (1989d) Localization, quantification and characterization of pancreatic polypeptide immunoreactivity in the parasitic flatwormDiclidophora merlangi and its fish host (Merlangius merlangus). Gen Comp Endocrinol 74:50–56
Maule AG, Shaw C, Halton DW, Johnston CF, Fairweather I, Buchanan KD (1989e) Tachykinin immunoreactivity in the parasitic flatwormDiclidophora merlangi and its fish host the withing (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera. Comp Biochem Physiol [C] 94:533–541
Osborne NN, Cuello AC, Dockray GJ (1982) Substance P and cholecystokinin-like peptides inHelix neurons and cholecystokinin and serotonin in a giant neuron. Science 216:409–411
O'Shea M, Schaffer M (1985) Neuropeptide function: the invertebrate contribution. Ann Rev Neurosci 8:171–198
Platt N, Reynolds SE (1988) Invertebrate neuropeptides. In: Lunt GG, Olsen RW (eds) Comparative invertebrate neurochemistry, ch 5. Croom Helm Ltd, Beckenham, pp 175–226
Rennison BD (1953) A morphological and histochemical study of egg shell formation inDiclidophora merlangi Kühn. Dissertation, Trinity College, Dublin
Reuter M (1987) Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system ofGyrodactylus salaris (Monogenea). Acta Zool (Stockh) 68:187–193
Reuter M (1988) Development and organisation of nervous systems visualized by immunocytochemistry in three flatworm species. Prog Zool 36:181–184
Reuter M, Palmberg I (1987) An ultrastructural and immunocytochemical study of gastrodermal cell types inMicrostomum lineare (Turbellaria, Macrostomida). Acta Zool (Stockh) 68:153–163
Reuter M, Palmberg I (1989) Development and differentiation of neuronal subsets in asexually reproducingMicrostomum lineare. Histochem 91:123–131
Reuter M, Karlin T, Schot LPC (1984) Immunocytochemical demonstration of peptidergic neurons in the central and peripheral nervous system of the flatwormMicrostomum lineare with antiserum to FMRF-amide. Cell Tissue Res 238:431–436
Reuter M, Wikgren M, Lehtonen M (1986) Immunocytochemical demonstration of 5-HT-like and FMRF-amide-like substances in whole mounts ofMicrostomum lineare (Turbellaria). Cell Tissue Res 246:7–12
Reuter M, Lehtonen M, Wikgren M (1988) Immunocytochemical evidence of neuroactive substances in flatworms of different taxa—a comparison. Acta Zool (Stockh) 69:29–37
Richard J, Klein MJ, Stoeckel ME (1989) Neural and glandular localization of substance P inEchinostoma caproni (Trematoda-Digenea). Parasitol Res 75:641–648
Roth J, Le Roith D, Lesniak MA, Pablo F de, Bassas L, Collier E (1986) Molecules of intercellular communication in vertebrates, invertebrates and microbes: do they share common orgins? Prog Brain Res 68:71–79
Scharrer B (1982) Peptidergic neurons. Acta Morphol Neerl Scand 20:219–223
Schilt J, Richoux JP, Dubois MP (1981) Demonstration of peptides immunologically related to vertebrate neurohormones inDugesia lugubris (Turbellaria, Tricladida). Gen Comp Endocrinol 43:331–335
Smyth JD (1976) Introduction to animal parasitology, 2nd edn. Hodder and Stoughton, London Sydney Auckland Toronto
Smyth JD, Halton DW (1983) The physiology of trematodes. Cambridge University Press, Cambridge
Thorndyke MC, Whitfield PJ (1987) Vasoactive intestinal polypeptide-like immunoreactive tegumental cells in the digenean helminthEchinostoma liei: possible role in host-parasite interactions. Gen Comp Endocrinol 68:202–207
Threadgold LT, Irwin SWB (1970) Electron microscope studies ofFasciola hepatica: IX. The fine structure of Mehlis' gland. Z Parasitenkd 35:16–30
Tramu G, Leonardelli J, Dubois MP (1977) Immunohistochemical evidence for an ACTH-like substance in hypothalamic LH-RH neurons. Neurosci Lett 6:305–309
Vanderhaeghen JJ, Lotstra F, Liston DR, Rossier J (1983) Proenkephalin, [met]enkephalin, and oxytocin immunoreactivities are localized in bovine hypothalamic magnocellular neurons. Proc Natl Acad Sci USA 80:5139–5143
Venturini G, Carolei A, Palladini G, Margotta V, Lauro MG (1983) Radioimmunological and immunocytochemical demonstration of met-enkephalin in planaria. Comp Biochem Physiol [C] 74:23–25
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
Wikgren M, Reuter M (1985) Neuropeptides in a microturbellarian — whole-mount immunocytochemistry. Peptides 6 [Suppl 3]:471–475
Wikgren M, Reuter M, Gustafsson M (1986) Neuropeptides in free-living and parasitic flatworms. An immunocytochemical study. Hydrobiologia 132:93–99
Williams JB (1960) The dimorphism ofPolystomum integerrimum (Frolich) Rudolphi and its bearing on relationships within the Polystomatidae: part I. J Helminthol 34:151–192
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Maule, A.G., Halton, D.W., Johnston, C.F. et al. 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 (1990). https://doi.org/10.1007/BF00933549
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DOI: https://doi.org/10.1007/BF00933549