Abstract
The localisation and distribution of neuropeptides in the peripheral nervous system of the pig roundwormAscaris suum have been determined by an indirect immunofluoresence technique in conjunction with confocal microscopy. Of the 31 antisera tested, immunostaining was obtained only with antisera to peptide YY (PYY), pancreatic polypeptide (PP) and FMRFamide. Immunostaining for PYY and FMRFamide was evident in the amphidial and papillary ganglia associated with the anterior nerve ring and in the nerves from these ganglia that terminated in sensory receptors within the buccal lips of the parasite. The only peptide immunoreactivity (IR) observed in the reproductive system of either sex was that evident in the nerve supply to the distal region of the vagina in the female worm. It took the form of a well-developed plexus of parallel nerve fibres, cross-connectives and looped commissures. The nerve net diminished in the more proximal region of the vagina. PP-IR was less intense than that for PYY and FMRFamide and was more restricted in distribution, being confined to a small number of nerve fibres in the nerve supply to the vagina; it did not occur in the nerves supplying the anterior sensory receptors. The possible roles of neuropeptides in the sensory and reproductive biology of nematodes are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Atkinson HJ, Isaac RE, Harris PD, Sharpe CM (1988) FMRFamide-like immunoreactivity within the nervous system of the nematodesPanagrellus redivivus, Caenorhabditis elegans andHeterodera glycines. J Zool 216:663–671
Brownlee DJA, Fairweather I, Johnston CF, Smart D, Shaw C, Halton DW (1993) Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm,Ascaris suum (Nematoda, Ascaroidea). Parasitology (in press)
Bullock TH (1965) Pseudocoelomate phyla: Acanthocephala, Rotifera, Gastrotricha, Kinorhyncha, Nematoda, Nematomorpha, and Entoprocta. In: Bullock TH, Horridge GA (eds) Structure and function in the nervous systems of invertebrates. W.H. Freeman and Company, San Franscisco London, pp 597–629
Chitwood BG, Chitwood MB (1974) The nervous system. In: Chitwood BG, Chitwood MB (eds) Introduction to nematology. University Park Press, Baltimore, pp 160–174
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
Cowden C, Stretton AOW, Davis RC (1989) AFI, a sequenced bioactive neuropeptide isolated from the nematodeAscaris suum. Neuron 2:1465–1473
Croll NA (1975) Indolealkylamines in the coordination of nematode behavioral activities. Can J Zool 53:894–903
Davenport TRB, Lee DL, Isaac RE (1988) Immunocytochemical demonstration of a neuropeptide inAscaris suum (Nematoda) using an antiserum to FMRFamide. Parasitology 97:81–88
Davenport TRB, Isaac RE, Lee DL (1991) The presence of peptides related to the adipokinetic hormone/red pigment-concentrating hormone family in the nematode,Panagrellus redivivus. Gen Comp Endocrinol 81:419–425
Davey KG (1964) Neurosecretory cells in a nematode,Ascaris lumbricoides. Can J Zool 42:731–734
Davey KG (1966) Neurosecretion and molting in some parasitic nematodes. Am Zool 6:243–249
Goh SL, Davey KG (1976a) Acetylcholinesterase and synapses in the nervous system ofPhocanema decipiens (Nematoda): a histochemical and ultrastructural study. Can J Zool 54:752–771
Goh SL, Davey KG (1976b) Selective uptake of noradrenaline, DOPA, and 5-hydroxytryptamine by the nervous system ofPhocanema decipiens (Nematoda): a light autoradiographic and ultrastructural study. Tissue and Cell 8:421–435
Goh SL, Davey KG (1985) Occurrence of noradrenaline in the central nervous system ofPhocanema decipiens and its possible role in the control of ecdysis. Can J Zool 63:475–479
Goldschmidt R (1903) Histologische Untersuchungen an Nematoden. I. Die Sinnesorgane vonAscaris lumbricoides L. undAscaris megalocephala (Clequ.). Zool Jahrb 18:1–57
Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD (1982) Serotonin and octopamine in the nematodeCaenorhabditis elegans. Science 216:1012–1014
Johnson CD, Stretton AOW (1987) GABA-immunoreactivity in inhibitory motor neurons of the nematodeAscaris. J Neurosci 7:223–235
Johnston CF, Shaw C, Halton DW, Fairweather I (1990) Confocal scanning laser microscopy and helminth neuroanatomy. Parasitol Today 6:305–308
Leach L, Trudgill DL, Gahan PB (1987) Immunocytochemical localization of neurosecretory amines and peptides in the free-living nematode,Goodeyus ulmi. Histochem J 19:471–475
Lee DL (1962) The distribution of esterase enzymes inAscaris lumbricoides. Parasitology 52:241–260
Lee DL (1973) Evidence for a sensory function for the copulatory spicules of nematodes. J Zool Lond 169:281–285
Lui A, Bečejac S, Krvavica S, Ćorić D (1963) On the activity and localization of cholinesterase inAscaris suum Goetz. Vet Arh 33:307–311
McLaren DJ (1976a) Nematode sense organs. Adv Parasitol 14:195–265
McLaren DJ (1976b) Sense organs and their secretions. In: Croll NA (ed) The organization of nematodes. Academic Press, London, pp 139–161
Omar MS, Kuhlow F (1977) Cholinesterase activity in the microfilaria ofWuchereria bancrofti Cobbold. Tropenmed Parasitol 28:467–470
Ramisz A (1965) Studies on the nervous system of nematodes by means of histochemical method for active acetylcholinesterase. I.Trichinella spiralis andSyphacia obvelata. Acta Parasitol Pol 13:205–212
Rapson EB, Chilwan AS, Jenkins DC (1986) Acetylcholinesterase secretion — a parameter for the interpretation ofin vitro anthelimintic screens. Parasitology 92:425–430
Reger JF (1965) The fine structure of neuromuscular junctions and contact zones between body wall muscle cells ofAscaris lumbricoides (var.suum). Z Zellforsch 67:196–210
Schinkmann K, Li C (1992) Localization of FMRFamide-like peptides inCaenorhabditis elegans. J Comp Neurol 316:251–260
Sharpe MJ, Atkinson HJ (1980) Improved visualization of dopaminergic neurons in nematodes using the glyoxylic acid fluorescence method. J Zool Lond 190:273–284
Sharpe MJ, Atkinson HJ, Trett MW, Lee DL (1980) Visualization of neurotransmitters in nematodes. In: Van den Bossche H (ed) The host invader interplay. Elsevier/North-Holland, Amsterdam, pp 713–716
Sithigorngul P, Stretton AOW, Cowden C (1990) Neuropeptide diversity inAscaris: an immunocytochemical study. J Comp Neurol 294:362–376
Stretton A, Donmoyer J, Davis R, Meade J, Cowden C, Sithigorngul P (1992) Motor behavior and motor nervous system function in the nematodeAscaris suum. J Parasitol 78:206–214
Sulston J, Dew M, Brenner S (1975) Dopaminergic neurons in the nematodeCaenorhabditis elegans. J Comp Neurol 163:215–226
Warbrick EV, Rees HH, Howells RE (1992) Immunocytochemical localisation of an FMRFamide-like peptide in the filarial nematodesDirofilaria immitis andBrugia pahangi. Parasitol Res 78:252–256
Wright KA (1974) Cephalic sense organs of the parasitic nematodeCapillaria hepatica (Bancroft, 1893). Can J Zool 10:1207–1213
Yeates RA, Ogilvie BM (1976) Nematode acetylcholinesterases. In: Van den Bossche H (ed) Biochemistry of parasites and host-parasite relationships. Elsevier/North-Holland, Amsterdam, pp 307–310
Yuen PH (1971) Electron microscope studies onAphelenchoides blastophthoras (Nematoda). I. The female genital tube. Nematologica 17:1–12
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Brownlee, D.J.A., Fairweather, I. & Johnston, C.F. Immunocytochemical demonstration of neuropeptides in the peripheral nervous system of the roundwormAscaris suum (Nematoda, ascaroidea). Parasitol Res 79, 302–308 (1993). https://doi.org/10.1007/BF00932186
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00932186