Morphological and Functional Characteristics of the Trematode Fasciola hepatica Musculature
- Authors: Kreshchenko N.D1
-
Affiliations:
- Institute of Cell Biophysics, Russian Academy of Sciences
- Issue: Vol 69, No 6 (2024)
- Pages: 1279-1290
- Section: Complex systems biophysics
- URL: https://kld-journal.fedlab.ru/0006-3029/article/view/676181
- DOI: https://doi.org/10.31857/S0006302924050134
- EDN: https://elibrary.ru/NKPTBW
- ID: 676181
Cite item
Abstract
The morphological structure and functional properties of musculature of flatworms Fasciola hepatica (Trematoda, Fasciolidae), parasites dangerous for agricultural animals and humans, have been studied. The histochemical staining of the body wall muscles of F. hepatica with fluorescently-labelled phalloidin has been performed and the stained samples were examined by fluorescent microscopy. Staining was observed both in longitudinal, circular, and diagonal muscle fibers of the body wall of the trematode, in the circular and diagonal muscle fibers surrounding the lumens of the branched intestine, and in the tubular structures of the reproductive tract. In the ventral and oral suckers of the trematode, tightly packed and intensively stained layers of muscle fibers were found. The physiological studies were conducted on the muscle strips prepared from F. hepatica. The results demonstrated that muscle preparations exhibit spontaneous contractile activity. Neuropeptide GYIRF, belonging to the FMRFamide-like peptide family, used at concentrations ranging from 1 µm to 10 µm, additionally stimulated the contractions of muscle preparations in F. hepatica, increasing the frequency and amplitude of contractions compared to their basic activity. The information obtained will be used in further investigation of muscle contraction mechanism in parasitic worms, the muscles of which are targets of antiparasitic drugs.
About the authors
N. D Kreshchenko
Institute of Cell Biophysics, Russian Academy of Sciences
Email: nkreshch@rambler.ru
Pushchino, Russia
References
- Бронштейн А. М., Малышев Н. А., Федянина Л. В. и Давыдова И. В. Фасциолез с длительным бессимптомным течением у больного из Туркменистана, осложнившийся острой механической желтухой: описание случая и обзор литературы. Эпидемиология и инфекционные болезни, 21 (2), 92—98 (2016).
- Сафиуллин Р. Т. Распространение и экономический ущерб от основных гельминтозов жвачных животных. Ветеринария, 6, 28—32 (1997).
- Alba A., Grech-Angelini S., Vázquez A. A., Alda P., Blin Q., Lemmonier L., Chauvin A., Chartier C., Douchet P., Hurtrez-Boussès S., Rey O., Foata J., Boissier J., and Quilichini Y. Fasciolosis in the mediterranean island of Corsica (France): insights from epidemiological and malacological investigations. Food Waterborne Parasitol., 30, e00188 (2023). doi: 10.1016/j.fawpar.2023.e00188
- Nyagura I., Malatji M. P., and Mukaratirwa S. Occurrence of Fasciola (Digenea: Fasciolidae) species in livestock, wildlife and humans, and the geographical distribution of their intermediate hosts in South Africa — a scoping review. Front. Vet. Sci. 9, 935428 (2022). doi: 10.3389/fvets.2022.935428
- Романенко Н. А., Горохов В. В., Сергиев В. П., Колесникова М. А., Успенский А. В., Молчанов И. А., Гурьева С. С. и Горохова Е. В. Заболеваемость фасциолезом человека. Медицинская паразитология и паразитарные болезни 2, 57—59 (2008).
- Никонорова М. А., Волчкова Е. В., Хорошилова И. А., Киушкина И. Н., Немилостива Е. А. и Арсеньева И. В., Трудности ранней диагностики у человека (описание клинического случая). Эпидемиология и инфекционные болезни, 1, 44—49 (2018).
- Теренина Н. Б. и Густафссон М. К. С, Функциональная морфология нервной системы паразитических плоских червей (Товарищество научных изданий КМК, М., 2014).
- Толстенков О. О., Прокофьев В. В., Теренина Н. Б., Галактионов К. В., Действие некоторых фармакологических веществ на двигательную активность церкарий Cryptocotyle lingua (Heterophyidae). Паразитология, 4, 346—370 (2010).
- Halton D. W. and Maule A. G. Flatworm nerve-muscle: structural and functional analysis. Can. J. Zool., 82, 316-333 (2004).
- Mair G. R., Maule A. G., Day T.A., and Halton D. W. A confocal microscopical study of the musculature of adult Schistosoma mansoni. Parasitology, 121 (2), 163170 (2000).
- Tolstenkov O. O., Terenina N. B., Serbina E. A., and Gustafsson M. K. S. The spatial relationship between the musculature and the 5-HT and FMRFamide-immunoreactivities in cercaria, metacercaria and adult Opisthorchis felineus (Digenea). Acta Parasitologica, 55, 123-132 (2010). doi: 10.2478/s11686-010-0024-4
- Terenina N. B., Kreshchenko N. D., Mochalova N. V., Nefedova D. V., Voropaeva E. L., Movsesyan S. O., Demiaszkiewicz A., Yashin V. A. and Kuchin A. V. The new data on the serotonin and FMRFamide localization in the nervous system of Opisthorchis felineus metacercariae. Acta Parasitologica, 65, 361-374 (2020). doi: 10.2478/s11686-019-00165-2
- Petrov A. and Podvyaznaya I. Muscle architecture during the course of development of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae) from cercariae to metacercariae. J. Helminthology, 90 (3), 321-336 (2016). doi: 10.1017/S0022149X15000310
- Крупенко Д. Ю. Пространственная организация мускулатуры церкарий Himasthla elongata (Trematoda: Echinostomatidae). Паразитология, 45 (6), 449460 (2011).
- Krupenko D. Y. Muscle system of Diplodiscus subclavatus (Trematoda: Paramphistomida) cercariae, pre-ovigerous and ovigerous adults. Parasitol. Res., 113 (3), 941-952 (2014). doi: 10.1007/s00436-013-3726-3
- Salvador-Recatalà V. and Greenberg R. M. Calcium channels of schistosomes: unresolved questions and unexpected answers, Wiley Interdisciplinary Reviews: Membrane Transport and Signaling, 1 (1), 85-93 (2012). doi: 10.1002/wmts.19
- Graham M. K., McGeown J. G., and Fairweather I. Ionic mechanisms underlying spontaneous muscle contractions in the liver fluke, Fasciola hepatica. Am. J. Physiol., 277, R374-R383 (1999). doi: 10.1152/ajpregu.1999.277.2.R374
- Hrckova G., Velenbny S., Halton D. W., and Maule A. G. Mesocestoides corti (syn. M. vogae): modulation of larval motility by neuropeptides, serotonin and acetylcholine, Parasitology, 124, 409-421 (2002). doi: 10.1017/s0031182001001329
- Novozhilova E., Kimber M. J., Qian H., McVeigh P., Robertson A. P., Zamanian M., Maule A. G., Day T. A. FMRFamide-like peptides (FLPs) enhance voltagegated calcium currents to elicit muscle contraction in the human parasite Schistosoma mansoni. PLoS Negl. Trop. Dis., 4 (8), e790 (2010). doi: 10.1371/journal.pntd.0000790
- Wang W., Wang L., and Liang Y. S. Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitol. Res., 111, 1871-1877 (2012). doi: 10.1007/s00436-012-3151-z
- Greenberg R., Ca2+ signalling, voltage-gated Ca2+channels and praziquantel in flatworm neuromusculature. Parasitology, S131 (1), 97-108 (2005). doi: 10.1017/S0031182005008346
- Fairweather I., Brennan G. P., Hanna R. E. B., Robinson M. W., and Skuce P. J. Drug resistance in liver flukes. Int. J. Parasitol. Drugs Drug. Resist., 12, 39-59 (2020). doi: 10.1016/j.ijpddr.2019.11.003
- Kreshchenko N. D. and Maule A. G., Investigation of peptide-induced and spontaneous and muscle activity in parasitic worm, a liver fluke, Fasciola hepatica. In Proc. Int. Symp. “Biological Motility: Basic Research and Practice” (Pushchino, 2006), pp. 28-29.
- Fellowes R. A., Maule A. G., Marks N. J., Geary T. G., Thompson D. P. and Halton D. W., Modulation of the motility of the vagina vera of Ascaris suum in vitro by FMRFamide-related peptides. Parasitology, 116, 277287 (1998).
- Mousley A., Marks N. J., Halton D. W., Geary T. G., Thompson D. P., and Maule A. G. Arthropod FMR-Famide-related peptide modulated muscle activity in helminths. Int. J. Parasitol., 34, 755-768 (2004).
- Wieland T. Modification of actins by phallotoxins. Naturwiss., 64, 303-309 (1977). doi: 10.1007/BF00446784
- Pollard T. D. and Weihing R. R., Actin and myosin and cell movement. CRC Crit. Rev. Biochem., 2 (1), 1-65 (1974). doi: 10.3109/10409237409105443.
- Matthews J. B., Tally K. J., Smith J. A., and Awtrey C. S., F-actin differentially alters epithelial transport and barrier function. J. Surg. Res., 56, 505-509 (1994). doi: 10.1006/jsre.1994.1081
- Chazotte B. Labeling cytoskeletal F-actin with rhodamine phalloidin or fluorescein phalloidin for imaging. Cold Spring Harb. Protoc., 5, pdb.prot4947 (2010). doi: 10.1101/pdb.prot4947
- Rieger R., Salvenmoser W., Legniti A., Reindl S., Adam H., Simonsberger P., and Tyler S., Organization and differentiation of the body-wall musculature in Macrostomum (Turbellaria, Macrostomidae). Hydrobiologia, 227, 119-129 (1991). doi: 10.1007/BF00027591
- Wahlberg M. H. The distribution of F-actin during the development of Diphyllobothrium dendriticum (Cestoda). Cell Tiss. Res., 291 (3), 561-570 (1998). doi: 10.1007/s004410051025
- Stitt A. W., Fairweather I., Trudgett A. G., Johnston C. F., and Anderson S. M. L. Localisation of actin in the liver fluke, Fasciola hepatica. Parasitol. Res., 78, 96-102 (1992).
- Mair G. R., Maule A. G., Shaw C., Johnston C. F. and Halton D. W. Gross anatomy of the muscle systems of Fasciola hepatica as visualized by phalloidin-fluorescence and confocal microscopy. Parasitology, 117, 7582 (1998).
- Stewart M. T., Marks N. J., and Halton D. W., Neuroactive substances and associated major muscle systems in Bucephaloides gracilescens (Trematoda: Digenea) metacercaria and adult. Parasitol. Res., 91 (1), 12—21 (2003).
- Kumar D., McGeown J. G., Reynoso-Ducoing O., Ambrosio J. R., and Fairweather I., Observations on the musculature and isolated muscle fibres of the liver fluke, Fasciola hepática. Parasitology, 127, 457—473 (2003). doi: 10.1017/s0031182003003925
- Maule A. G., Shaw C., Halton D. W., and Tim L., GNFFRFamide: a novel FMRFamide-immunoreactive pepetide isolated from the sheep tapeworm Moniezia expansa. Biochem. Biophys. Res. Comm., 193 (3), 1054-1060 (1993).
- Maule A. G., Shaw C., Halton D. W., Curry W. J., and Thim L. RYIRFamide: a turbellarian FMRFamide-related peptide (FaRP). Regul. Pept. 50, 37-43 (1994).
- Johnston R. N., Shaw C., Halton D. W., Verhaert P., and Baguna J., GYIRFamide: a novel FMRFamide-related peptide (FaRP) from the triclad turbellarian, Dugesia tigrina. Biochem. Biophys. Res. Comm., 209 (2), 689-697 (1995).
- Johnston R. N., Shaw C., Halton D. W., Verhaert P., Blair K. L., Brennan G. P., Price D. A. and Anderson P. Isolation, localization, and bio-activity of the FMRFamide- related neuropeptides GYIRFamide and YIRFamide from marine turbellarian Bdelloura candida. J. Neurochem., 67, 814-821 (1996).
- Крещенко Н. Д. Пептидергическая сигнализация: иммуноцитохимическое определение FMRF-подобных пептидов в нервной системе планарий. Биол. мембраны, 30 (5-6), 430-437 (2013). doi: 10.7868/S0233475513050095
- Magee R. M., Fairweather I., Johnston C. F., Halton D. W. and Shaw C. Immunocytochemical demonstration of neuropeptides in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology, 98 (2), 227-238 (1989). doi: 10.1017/s0031182000062132
- Marks N. J., Halton D. W., Maule A. G. Brennan G. P., Shaw C., Southgate V. R. and Johnston C. F. Comparative analyses of the neuropeptide F (NPF)- and FMRFamide-related peptide (FaRP)-immunoreactiv-ities in Fasciola hepatica and Schistosoma spp. Parasitology, 110 (4), 371-381 (1995).
- Brownlee D. J., Brennan G. P., Halton D. W., Fairweather I., and Shaw C. Ultrastructural localisation of FMRFamide- and pancreatic polypeptide-immunoreactivities within the central nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitol. Res. 80 (2), 117-124 (1994). doi: 10.1007/BF00933778
- Terenina N. B., Kreshchenko N. D., Mochalova N. V., and Movsesyan S. O., Serotonin and neuropeptide FMRFamide in the attachment organs of trematodes. Helminthologia, 55 (3), 185-194 (2018).
- Day T. A., Maule A. G., Shaw C., Halton D. W., Moore S., Bennet J. L. and Pax R. A., Platyhelminth FMRFamide-related peptides (FaRPs) contract Schistosoma mansoni (Trematoda: Digenea) muscle fibres in vitro. Parasitology, 109, 455-459 (1994).
- Hrchkova G., Velebny S., Halton D. W., Day T. A., and Maule A. G. Pharmacological characterization of neuropeptide F (NPF)-induced effects on the motility of Mesocestoides corti (syn. Mesocestoides vogae) larvae. Int. J. Parasitol., 34, 83-93 (2004).
- Moneypenny C. G., Maule A. G., Shaw C., Day T. A., Pax R. A., and Halton D. W. Physiological effects of platyhelminth FMRFamide-related peptides (FaRPs) on the motility of the monogenean Diclidophora merlangi. Parasitology, 115 (3), 281-288 (1997). doi: 10.1017/s0031182097001364
- Marks N. J., Johnston C. F., Maule A. G., Halton D. W., Shaw C., Geary T. G., Moore S., and Thompson D. P. Physiological effects of platyhelminthes RFamide peptides on muscle-strip preparations of Fasciola hepatica (Trematoda: Digenea). Parasitology, 113, 393-401 (1996).
- Graham M. K., Fairweather I. and McGeown J. G. Second messengers mediating mechanical responses to the FARP GYIRFamide in the fluke Fasciola hepatica. Am. J. Physiol. Regul. Integr. Comp. Physiol., 279 (6), R2089-2094 (2000)
- Marks N. J., Maule A. G., Halton D. W., Geary T. G., and Shaw C., Pharmacological effects of nematode FMRFamide-related peptides (FaRPs) on muscle contractility of the trematode, Fasciola hepatica. Parasitology, 114, 531-539 (1997).
- Blair K. L., Day T. A., Lewis M. C., Bennet J. L., and PaxR. A. Studies on muscle cells isolated from Schistosoma mansoni. A Ca2+-dependent K+ channel. Parasitology, 102, 251-258 (1991).
- Day T. A., Maule A. G., Shaw C., and Pax R. A. Structure-activity relationships of FMRFamide-related peptides contracting Schistosoma mansoni muscle. Peptides, 18 (7), 917-921 (1997).
- Novozhilova E., Kimber M. J., Qian H., McVeigh P., Robertson A. P. , Zamanian M., Maule A. G,. and DayT. A. FMRFamide-like peptides (FLPs) enhance voltage-gated calcium currents to elicit muscle contraction in the human parasite Schistosoma mansoni. PLoS Negl. Trop. Dis., 4 (8), e790 (2010). doi: 10.1371/journal.pntd.000079
- Blair K. L. and Anderson P. A. Physiological and pharmacological properties of muscle cells isolated from the flatworm Bdelloura candida (Tricladia). Parasitology, 109, 325-335 (1994).
- Moneypenny C. G., Kreshchenko N., Moffett C. L., Halton D. W., Day T. A., and Maule A. G., Physiological effects of FMRFamide-related peptides and classical transmitters on dispersed muscle fibres of the turbellarian, Procerodes littoralis. Parasitology, 122 (4), 447-455 (2001). doi: 10.1017/s0031182001007508.
Supplementary files
