Abstract
Background
Trematoda Opisthorchis felineus Rivolta, 1884 is the causative agent of dangerous parasite disease—opisthorchiasis, widespread in the Russian Federation. The details of the neuroanatomical localization of the serotoninergic and FMRFamidergic neurotransmitter elements as well as their functional roles remain not studied enough in both adult and larval forms of O. felineus. The studies in this area are important in term of the development of a new pharmacological strategy of the struggle with the causative agent of opisthorchiasis affecting the neuronal signal substances and the function of its nervous system.
Purpose
The aim of this work was the immunocytochemical study of the neurotransmitters serotonin (5-HT, 5-Hydroxitryptamine) and neuropeptide FMRFamide localization in the nervous system of the opisthorchiasis causative agent—O. felineus metacercaria. To study the relationship between the detected neurotransmitters and the muscular elements of the parasite, the muscle staining was carried out simultaneously using fluorophore-conjugated phalloidin.
Methods
The localization of 5-HTergic and FMRFamidergic nerve structures was determined by immunocytochemical method. The staining samples were analyzed using a fluorescent and confocal laser scanning microscopies.
Results
The new data on the presence and distribution of the serotonin-immunopositive (IP)- and FMRFa-IP components in the central and peripheral departments of the nervous system of O. felineus metacercaria has been obtained. Besides that a number of the new anatomical details of the nervous system organization and of the innervation of the organs and tissues in the investigated parasite have been revealed.
Conclusion
The data obtained on the presence and localization of the 5-HTergic and peptidergic (FMRFamide) components in central and peripheral departments of the nervous system of O. felineus metacercaria elaborated and expanded the existing information about the nervous system as well as the innervations of the tissues and organs in the causative agent of opistchorchiasis.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.2478%2Fs11686-019-00165-2/MediaObjects/11686_2019_165_Fig1_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.2478%2Fs11686-019-00165-2/MediaObjects/11686_2019_165_Fig2_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.2478%2Fs11686-019-00165-2/MediaObjects/11686_2019_165_Fig3a_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.2478%2Fs11686-019-00165-2/MediaObjects/11686_2019_165_Fig3b_HTML.jpg)
Similar content being viewed by others
References
Andreini GC, Beretta C, Faustini R, Gallina G (1970) Spectrofluorometric and chromatographic characterization of a butanol extract from Fasciola hepatica. Experientia 26(2):166–167
Arkhipov IA (2009) Anthelmintics: Pharmacology and application, Moscow. pp 405 (In Russian)
Barton ChL, Halton DV, 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. https://doi.org/10.1007/BF00931828
Beer SA (2005) Biology of the opisthorchiasis agent. Moscow, KMK, p 336 (In Russian)
Bennett J, Bueding E, Timms AR, Engstrom RG (1969) Occurrence and levels of 5-hydroxytryptamine in Schistosoma mansoni. Mol Pharmacol 5:542–545
Bennett J, Bueding E (1971) Localization of biogenic amines in Schistosoma mansoni. Compar Biochem Physiol 39(4):859–867
Catto BA, Ottesen EA (1979) Serotonin uptake in schistosomules of Schistosoma mansoni. Compar Biochem Physiol 63C(2):235–242
Chou TCT, Bennett J, Bueding E J (1972) Occurrence and concentrations of biogenic amines in trematodes. J Parasitol 58(6):1098–1102
Coons AH, Leduc EH, Connolly JM (1955) Studies of antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study for the hiperimmune rabbit. J Exper Med 102:49–60
Curry W J, Shaw C, Jonston C F, Thim L, Buchanan K D (1992) Neuropeptide F: primary structure from the turbellarian, Artioposthia triangulate. Comp Biochem Physiol Part C Pharmacol Toxicol Endocrinol 101:269–274
Del-Cas E, Dhainaut-Courtois N, Dhainaut A, Vernes A (1979) Ultrastructural localization of tritiated 5-HT in adult Schistosoma mansoni. A preliminary report. Biol Cellulaire 35:321–324
Dorsey C H, Cousin E (1986) Schistosoma mansoni: a new parenchima cell in cercariae. Expl Parasitol 61(1):33–41
Day TA, Maule AG (1999) Parasitic peptides! The structure and function of neuropeptides in parasitic worms. Peptides 20:999–1019
Fairweather I, Maule A G, Mitchell S H, Johnston C F, Halton D W (1987) Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitol Res 73(3):255–258
Galaktionov KV, Dobrovolskij AA (1998) The origin and evolution of Trematode life cycles. Sankt-Peterburg “Nauka”, 404 pp
Glaskov GA (1979) Isolation of some trematode metacercariae from diseased fish tissue by digestion in artificial gastric juice. Diseases and parasites of fish in the Litovitomsk province (within the USSR) Tomsk, pp.72–82 (In Russian)
Gustafsson M KS (1987) Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitol Res 74(2):168–174
Gustafsson MKS, Halton DW (2001) Nervous system of platyhelminthes. In: Mehlhorn H (ed) Encyclopedic reference in parasitology. Springer, Berlin, pp 423–439
Gustafsson MKS, Halton DW, Kreshchenko ND, Movsessian SO, Raikova OI, Reuter M, Terenina NB (2002) Neuropeptides in flatworms. Peptides 23:2053–2061
Halton D W, Gustafsson M KS (1996) Functional morphology of the platylhelminth nervous system. Parasitology 113(Suppl):47–72
Halton DW, Maule AG (2004) Flatworm nerve-muscle: structural and functional analysis. Can J Zool 82:316–333. https://doi.org/10.1139/z03-221
Johnston R N, Shaw C, Halton D W, Verhaert P, Bagunla J (1995) GYI.RFamide: a novel FMRFamide-related peptide (FaRP) from the triclad turbellarian, Dugesia tigrina. Biochem Biophys Res Commun 209:689–697
Johnston RN, Shaw C, Halton DW, Verhaert P, Blair K L, Brennan G P, Price D A, Anderson P A (1996) Isolation, localization, and bioactivity of the FMRFamide – related neuropeptides GYIRFamide and YIRFamide from marine turbellarian Bdelloura candida. J Neurochem 67:814–821
Koziol U, Koziol M, Preza M, Costabile A, Brehm K, Castillo E (2016) De novo discovery of neuropeptides in the genomes of parasitic 4 flatworms using a novel comparative approach. Int J Parasitol 46:709–721
Krupenko DY (2014) Muscle system of Diplodiscus subclavatus (Trematoda: Paramphistomida) cercariae, pre-ovigerous, and ovigerous adults. Parasitol Res 113:941–952. https://doi.org/10.1007/s00436-013-3726-3
Krupenko DY (2019) Oral sucker in Digenea: structure and muscular arrangement. Zoomorphology 138:29–37. https://doi.org/10.1007/s00435-018-0423-x
Krupenko DY, Dobrovolskij AA (2015) Somatic musculature in trematode hermaphroditic generation. BMC Evol Biol 15:189. https://doi.org/10.1186/s12862-015-0468-0
Krupenko D, Dobrovolskij AA (2018) Morphological framework for attachment and locomotion in several Digenea of the families Microphallidae and Heterophyidae. Parasitol Res 117(12):3799–3807. https://doi.org/10.1007/s00436-018-6085-2
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(2):227–238. https://doi.org/10.1017/S0031182000062132
Magee C A, Cahir M, Halton D W, Johnston C F, Shaw C (1993) Cytochemical observation on the nervous system of adult Corrigia vitta. J Helminthology 67(3):189–199
Mair G R, Maule A G, Day T A, Halton D W (2000) A confocal microscopical study of the musculature of adult Schistosoma mansoni. Parasitology 121:163–170
Mansour T AG (1984) Serotonin receptors in parasitic worms. Adv Parasitol 23:1–36
Mansour T E, Stone D B (1970) Biochemical effects of lysergic acid diethylamide on the liver fluke Fasciola hepatica. Biochem Pharmacol 19:1137–1146
Marks NJ, Halton DW, Maule AG, Brennan GP, Shaw C, Southgate VR, Johnston CF (1995) Comparative analyses of the neuropeptide F (NPF)- and FMRFamide-related peptide (FaRP)-immunoreactivities in Fasciola hepatica and Schistosoma spp. Parasitology 110:371–378
Maule A G, Shaw C, Halton D W, Thim L, Johnston S F, Fairweather I, Buchnan K D (1991) Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda, Cyclophyllidea). Parasitology 106:429–440
Maule A G, Shaw C, Halton D W, Thim L (1993) GNFFRFamide: a novel FMRFamide-immunoreactive peptide isolated from the sheep tapeworm, Moniezia expansa. Biochem Biophys Res Commun 193:1054–1060
Maule A G, Shaw C, Halton D W, Curry W J, Thim L (1994) RYIRFamide: a turbellarian FMRFamide-related peptide (FaRP). Regul Pept 50:37–43
McKay D M, Halton D W, Allen J M, Fairweather J (1989) The effects of cholinergic and serotoninergic drugs on motility in vitro of Halpometra cylindracea (Trematoda: Digenea). Parasitology 99:241–252
McKay D M, Halton D W, Johnston C F, Fairweather J, Shaw C (1990) Occurrence and distribution of putative neurotransmitters in the frog-lung parasite Haplometra cylindracea (Trematoda: Diginea). Parasitol Res 76(6):509–517
McKay D M, Halton DW, Maule AG, Johnston CF, Fairweather J, Shaw C (1991) Cytochemical demonstration of cholinergic, serotoninergic and peptidergic nerve elements in Gorgoderina vitelliloba (Trematoda: Digenea). J Parasitol 21:71–80
Mousley A, Maule AG, Halton DW, Marks NJ (2005) Inter-phyla studies on neuropeptides: the potential for broad-spectrum anthelmintic and/or endectocide discovery. Parasitology 131:143–167
McVeigh P, Kimber MJ, Novozhilova E, Day TA (2005) Neuropeptide signalling systems in flatworms. Parasitology 131:S41–S55
McVeigh P, Mair GR, Atkinson L, Ladurner P, Zamanian M, Novozhilova E, Marks NJ, Day TA, Maule AG (2009) Discovery of multiple neuropeptide families in the phylum Platyhelminthes. Int J Parasitol 39:1243–1252
Pax R A, Siefker C, Bennett J L (1984) Schistosoma mansoni: differences in acetylcholine, dopamine, and serotonin control of circular and longitudinal parasite muscle. Exp Parasitol 58:314–324
Petrov A, Podvyaznaya I (2016) Muscle architecture during the courseof development of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae) from cercariae to metacercariae. J Helminthol 90(3):321–326. https://doi.org/10.1017/S0022149X15000310
Petrov AA, Podvyaznaya IM, Zaitseva OV (2019) Architecture of the nervous system in metacercariae of Diplostomum pseudospathaceum Niewiadomska, 1984 (Digenea). Parasitol Res 118(4):1193–1203. https://doi.org/10.1007/s0043
Ribeiro P, El-Shehabi F, Patocka N (2005) Classical transmitters and their receptors in flatworms. Parasitology 131:S19–S40
Ŝebelová S, Stewart M, Mousley A, Fried B, Marks N, Halton DW (2004) The muscularture and associated innervation of adult and intramolluscan stages of Echinostoma caproni (Trematoda) visualized by confocal microscopy. Parasitol Res 93:196–206
Syskov TG, Tsybin TN, Sidorenk AG, Yasinsky AA (2001) The state of parasitic morbidity in the population of the Russian Federation in 1999. Med Parasitol Parasites Bol 3:31–35 (In Russian)
Skuce PJ, Johanston CF, Fairweather I, Halton DW, Shaw C (1990) A confocal scanning laser microscope study of the peptidergic and serotoninergic components of the nervous system in larval Schistosoma mansoni. Parasitology 101:227–234
Solovykh GN, Skachkov MV, Kanunikova EA, Nikitina LP, Vereshchagin NN (2007) Opisthorchiasis. M “Medicine”, 168 pp. (In Russian)
Stewart M T, Marks N J, Halton D W (2003) Neuroactive substances and associated major muscle systems in Bucephaloides gracilescens (Trematoda: Digenea) metacercariae and adult. Parasitol Res 91(1):12–21
Stewart MT, Mousley A, Koubková B, Šebelova Š, Marks N, Halton DW (2003) Gross anatomy of the muscle systems and associated innervation of Apatemon cobitidis proterorhini (Trematoda: Strigeidea), as visualized by confocal microscopy. Parasitology 126:273–282
Thompson CS, Mettrick DF (1989) The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Can J Zool 67:1257–1262
Terenina NB, Gustafsson MKS (2003): Neurotransmitters in helminths. Moscow, “Nauka”, 176 pp. (In Russian)
Terenina NB, Gustafsson MKS (2014) The Functional morphology of the nervous system of parasitic flatworms (Trematodes, Cestodes). KMK Scientific Press, Moscow, 296 pp. (In Russian)
Terenina NB, Tolstenkov O, Fagerholm HP, Serbina EA, Vodjanitskaja SN, Gustafsson MK (2006) The spatial relationship between the musculature and the NADPH-diaphorase activity, 5-HT and FMRFamide immunoreactivities in redia, cercaria and adult Echinoparyphium aconiatum (Digenea). Tissue Cell 38:151–157
Terenina N, Kreshchenko N, Mochalova N, Movsesyan S (2018) Serotonin and neuropeptide FMRFamide in the attachment organs of trematodes. Helminthologia 55(3):185–194. https://doi.org/10.2478/helm-2018-0022
Tolstenkov OO, Terenina NB, Serbina EA, Gustafsson MKS (2010) The spatial relationship between the musculature and the 5-HT and FMRFamide immunoreactivities in cercaria, metacercaria and adult Opisthorchis felineus (Digenea). Acta Parasitol 55(2):123–132
Wahlberg MH (1998) The distribution of F-actin during the development of Diphyllobothrium dendriticum (Cestoda). Cell Tissue Res 291(3):561–570
Yastrebov MV, Yastrebova IV (2014): Muscular system of trematodes. KMK Scientific Press Ltd, Moscow, 343 pp (In Rusian)
Yurlova NI, Yadrenkina EN, Rastyazhenko NM, Serbina EA, Glupov VV (2017) Opisthorchiasis in Western Siberia: Epidemiology and distribution in human, fish, snail, and animal populations. Parasitol Int 66:355–364
Zhu-Ge Rong Hua, Rong Yao-Fang (1988) Acta pharmacol sin 9(3):267–271
Acknowledgements
This work was supported by the Russian Foundation for Basic Research (Grant No.18-04-00349a to Kreshchenko ND, Terenina NB, Mochalova NV).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
Authors declare that they have no conflict of interest.
Ethical Approval
All procedures performed in the article “The new data on the serotonin and FMRFamide localization in the nervous system of Opisthorchis felineus metacercaria” involving animals were in accordance with the ethical standards of the Institution at which the studies were conducted.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Terenina, N.B., Kreshchenko, N.D., Mochalova, N.V. et al. The New Data on the Serotonin and FMRFamide Localization in the Nervous System of Opisthorchis felineus Metacercaria. Acta Parasit. 65, 361–374 (2020). https://doi.org/10.2478/s11686-019-00165-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11686-019-00165-2