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Observations on the musculature and isolated muscle fibres of the liver fluke, Fasciola hepatica

Published online by Cambridge University Press:  17 October 2003

D. KUMAR ,
J. G. McGEOWN ,
O. REYNOSO-DUCOING ,
J. R. AMBROSIO  and
I. FAIRWEATHER
D. KUMAR
Affiliation:
Parasite Proteomics and Therapeutics Research Group, School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT9 7BL, Northern Ireland Division of Pharmacology and Toxicology, Indian Veterinary Research Institute, Izatnagar – 243 122 (UP), India
J. G. McGEOWN
Affiliation:
Smooth Muscle Research Group, Department of Physiology, The Queen's University of Belfast, Belfast BT9 7BL, Northern Ireland
O. REYNOSO-DUCOING
Affiliation:
Department of Microbiology and Parasitology, School of Medicine, National Autonomous University of Mexico, Mexico City, Mexico 04510
J. R. AMBROSIO
Affiliation:
Department of Microbiology and Parasitology, School of Medicine, National Autonomous University of Mexico, Mexico City, Mexico 04510
I. FAIRWEATHER
Affiliation:
Parasite Proteomics and Therapeutics Research Group, School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT9 7BL, Northern Ireland
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Abstract

The liver fluke, Fasciola hepatica relies on a well-developed muscular system, not only for attachment, but for many aspects of its biology. Despite this, little is known about the system beyond the gross organization of the main somatic muscle layers. In the present study, a range of techniques have been applied to F. hepatica in order to understand more about various aspects of muscle organization, biochemistry (in terms of muscle proteins) and identity of isolated muscle fibres. Scanning electron microscopy has provided a direct visualization in situ of the somatic muscle layers and the organization of the muscle fibres within the ventral sucker. The muscle bundles contributing to the main somatic muscle layers are made up of up to 10 individual muscle fibres. Phalloidin staining for actin, in conjunction with confocal microscopy, confirmed the presence of 2 main somatic muscle layers (outer circular, inner longitudinal), beneath which lies a third layer of oblique muscle fibres. The use of propidium iodide in combination with phalloidin staining for actin demonstrated that the cell bodies associated with the 2 main somatic muscle layers are situated beneath the longitudinal muscle layer and are connected to their respective muscle fibres by short cytoplasmic processes. Myosin immunoreactivity was demonstrated in the somatic muscle layers and in the muscle layers surrounding various organ systems within the fluke. Double labelling for actin and myosin confirmed the co-localization of the 2 muscle proteins in the muscle fibres of the ventral sucker. Muscle fibres from the somatic muscle layers and the ventral sucker have been isolated and images obtained with phase-contrast microscopy and scanning electron microscopy. The muscle fibres contain actin and myosin, but lack a nucleus, the connection with the cell body having been broken during the isolation procedure.

Keywords

Fasciola hepaticamusculatureisolated muscle fibresactinmyosinelectron microscopyimmunocytochemistry
Type
Research Article
Information
Parasitology , Volume 127 , Issue 5 , November 2003 , pp. 457 - 473
Copyright
2003 Cambridge University Press

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References

REFERENCES

ABBAS, M. K. & CAIN, G. D. (1987). Actin and intermediate-sized filaments of the spines and cytoskeleton of Schistosoma mansoni. Parasitology Research 73, 66–74.CrossRefGoogle Scholar
ABBAS, M. K. & CAIN, G. D. (1989). Analysis of isoforms of actin from Schistosoma mansoni by two-dimensional gel electrophoresis. Parasitology Research 76, 178–180.CrossRefGoogle Scholar
ALEKSANDRYUK, S. P. (1964). Regulation of tone in plerocercoids of the tapeworm Ligula intestinalis. Doklady Akademii Nauk SSSR 157, 1249–1252.Google Scholar
AMBROSIO, J., CRUZ-RIVERA, M., ALLAN, J., MORAN, E., ERSFIELD, K. & FLISSER, A. (1997). Identification and partial characterization of a myosin-like protein from cysticerci and adults of Taenia solium using a monoclonal antibody. Parasitology 114, 545–553.Google Scholar
BAGUNA, J. & ROMERO, R. (1981). Quantitative analysis of cell types during growth, degrowth and regeneration in the planarians Dugesia mediterranea and Dugesia tigrina. Hydrobiologia 84, 181–194.CrossRefGoogle Scholar
BECKER, M. M., KALINNA, B. H., YANG, W., HARROP, S. A., SCOTT, J. C., WAINE, G. J., KURTIS, J. D. & McMANUS, D. P. (1995). Gene cloning and complete nucleotide sequence of Philippine Schistosoma mansoni paramyosin. Acta Tropica 59, 143–147.CrossRefGoogle Scholar
BLAIR, K. L. & ANDERSON, P. A. V. (1994). Physiological and pharmacological properties of muscle cells isolated from the flatworm Bdelloura candida (Tricladida). Parasitology 109, 325–335.CrossRefGoogle Scholar
BLAIR, K. L., DAY, T. A., LEWIS, M. C., BENNETT, J. L. & PAX, R. A. (1991). Studies on muscle cells isolated from Schistosoma mansoni: a Ca2+-dependent K+ channel. Parasitology 102, 251–258.CrossRefGoogle Scholar
CAMPOS, A., BERNARD, P., FAUCONNIER, A., LANDA, A., GOMEZ, E., HERNANDEZ, R., WILLMS, K. & LACLETTE, J. P. (1990). Cloning and sequencing of two actin genes from Taenia solium (Cestoda). Molecular and Biochemical Parasitology 40, 87–94.CrossRefGoogle Scholar
CAROLEI, A., MARGOTTA, V. & PALLADINI, G. (1975). Proposal of a new model with dopaminergic-cholinergic interactions for neuropharmacological investigations. Neuropsychobiology 1, 355–364.CrossRefGoogle Scholar
CEBRIA, F., VISPO, M., NEWMARK, P., BUENO, D. & ROMERO, R. (1997). Myocyte differentiation and body wall muscle regeneration in the planarian Girardia tigrina. Development Genes and Evolution 207, 306–316.CrossRefGoogle Scholar
CHAPMAN, H. D. (1973). The functional organization and fine structure of the tail musculature of the cercariae of Cryptocotyle lingua and Himasthla secunda. Parasitology 66, 487–497.CrossRefGoogle Scholar
CHIEN, P. & KOOPOWITZ, H. (1972). The ultrastructure of neuromuscular systems in Notoplana acticola, a free-living polyclad flatworm. Zeitschrift für Zellforschung und Mikroskopische Anatomie 133, 277–288.CrossRefGoogle Scholar
COONS, A. H., LEDUC, E. H. & CONNOLLY, J. M. (1955). Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyper-immune rabbit. Journal of Experimental Medicine 102, 49–60.Google Scholar
CRISSMAN, H. A. & STEINKAMP, J. A. (1973). Rapid, simultaneous measurement of DNA, protein, and cell volume in single cells from large mammalian cell populations. Journal of Cell Biology 59, 766–771.CrossRefGoogle Scholar
DA SILVA, C. M. D., FERREIRA, H. B., PICON, M., GORFINKIEL, N., EHRLICH, R. & ZAHA, A. (1993). Molecular cloning and characterization of actin genes from Echinococcus granulosus. Molecular and Biochemical Parasitology 60, 209–220.CrossRefGoogle Scholar
DAVIS, A. H., BLANTON, R. & KLICH, P. (1985). Stage and sex specific differences in actin gene expression in Schistosoma mansoni. Molecular and Biochemical Parasitology 17, 289–298.CrossRefGoogle Scholar
DAY, T. A., KIM, E., BENNETT, J. L. & PAX, R. A. (1995). Analysis of the kinetics and voltage-dependency of transient and delayed K+ currents in muscle fibers isolated from the flatworm Schistosoma mansoni. Comparative Biochemistry and Physiology 111A, 79–87.CrossRefGoogle Scholar
DAY, T. A., ORR, N., BENNETT, J. L. & PAX, R. A. (1993). Voltage-gated currents in muscle cells of Schistosoma mansoni. Parasitology 106, 471–477.CrossRefGoogle Scholar
DISSOUS, C., TORPIER, G., DUVAUX-MIRET, O. & CAPRON, A. (1990). Structural homology of tropomyosins from the human trematode Schistosoma mansoni and its intermediate host Biomphalaria glabrata. Molecular and Biochemical Parasitology 43, 245–256.CrossRefGoogle Scholar
FAIRWEATHER, I., HOLMES, S. D. & THREADGOLD, L. T. (1983). Fasciola hepatica: a technique for monitoring in vitro motility. Experimental Parasitology 56, 369–380.CrossRefGoogle Scholar
FAIRWEATHER, I., THREADGOLD, L. T. & HANNA, R. E. B. (1999). Development of Fasciola hepatica in the mammalian host. In Fasciolosis (ed. Dalton, J. P.), pp. 47–111. CAB International, Wallingford, Oxon.
FERRER, J., GONZALEZ-MORENO, O. & GRACENEA, M. (2001). Actin cytoskeleton in adults and metacercariae of Brachylaima sp. Journal of Helminthology 75, 337–344.Google Scholar
FETTERER, R. H., PAX, R. A. & BENNETT, J. L. (1977). Schistosoma mansoni: direct method for simultaneously recording of electrical and motor activity. Experimental Parasitology 43, 286–294.CrossRefGoogle Scholar
GOBERT, G. N., STENZEL, D. J., JONES, M. K., ALLEN, D. E. & McMANUS, D. P. (1997). Schistosoma japonicum: immunolocalization of paramyosin during development. Parasitology 114, 45–52.CrossRefGoogle Scholar
GRAHAM, M. K., FAIRWEATHER, I. & McGEOWN, J. G. (1997). The effects of FaRPs on the motility of isolated muscle strips from the liver fluke, Fasciola hepatica. Parasitology 114, 455–465.CrossRefGoogle Scholar
GRAHAM, M. K., FAIRWEATHER, I. & McGEOWN, J. G. (2000). Second messengers mediating mechanical responses to the FaRP GYIRFamide in the fluke Fasciola hepatica. American Journal of Physiology 279, R2089–R2094.CrossRefGoogle Scholar
GRAHAM, M. K., McGEOWN, J. G. & FAIRWEATHER, I. (1999). Ionic mechanisms underlying spontaneous muscle contractions in the liver fluke, Fasciola hepatica. American Journal of Physiology 277, R374–R383.CrossRefGoogle Scholar
GROSSMAN, Z., RAM, D., MARKOVICS, A., TARRAB-HAZDAI, R., LANTNER, F. & SCHECHTER, I. (1990). Schistosoma mansoni: stage-specific expression of muscle-specific genes. Experimental Parasitology 70, 62–71.CrossRefGoogle Scholar
HARLOW, E. & LANE, D. (1988). Antibodies. A Laboratory Manual. Cold Spring Harbor, New York.
HOOGE, M. D. & TYLER, S. (1999). Body-wall musculature of Praeconvoluta tornuva n.sp. (Acoela, Platyhelminthes) and the use of muscle patterns in taxonomy. Invertebrate Biology 118, 8–17.Google Scholar
ISHII, A. I. & SANO, M. (1980). Isolation and identification of paramyosin from liver fluke muscle layer. Comparative and Biochemical Physiology 65B, 537–541.CrossRefGoogle Scholar
JOHNSTON, R. N., SHAW, C., HALTON, D. W., VERHAERT, P., BLAIR, K. L., BRENNAN, G. P., PRICE, D. A. & ANDERSON, P. A. V. (1996). Isolation, localization, and bioactivity of the FMRFamide-related neuropeptides GYIRFamide and YIRFamide from the marine turbellarian Bdelloura candida. Journal of Neurochemistry 67, 814–821.CrossRefGoogle Scholar
KOBAYASHI, C., KOBAYASHI, S., ORII, H., WATANABE, K. & AGATA, K. (1998). Identification of two distinct muscles in the planarian Dugesia japonica by their expression of myosin heavy chain genes. Zoological Science 15, 861–869.CrossRefGoogle Scholar
KRISHNAN, A. (1975). Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. Journal of Cell Biology 66, 188–193.CrossRefGoogle Scholar
LACLETTE, J. P., MERCHANT, M. T. & WILLMS, K. (1987). Histological and ultrastructural localization of antigen B in the metacestode of Taenia solium. Journal of Parasitology 73, 121–129.CrossRefGoogle Scholar
LACLETTE, J. P., SKELLY, P. J., MERCHANT, M. T. & SHOEMAKER, C. B. (1995). Aldehyde fixation dramatically alters the immunolocalization pattern of paramyosin in platyhelminth parasites. Experimental Parasitology 81, 140–143.CrossRefGoogle Scholar
LANDA, A., LACLETTE, J. P., NICHOLSON-WELLER, A. & SHOEMAKER, C. B. (1993). cDNA cloning and recombinant expression of collagen-binding and complement inhibitor activity of Taenia solium paramyosin (AgB). Molecular and Biochemical Parasitology 60, 343–348.CrossRefGoogle Scholar
LINCKS, J., BOYAN, B. D., BLANCHARD, C. R., LOHMANN, C. H., LIU, Y., COCHRAN, D. L., DEAN, D. D. & SCHWARTZ, Z. (1998). Response of MG63 osteoblast-like cells to titanium and titanium alloy is dependent on surface roughness and composition. Biomaterials 19, 2219–2232.CrossRefGoogle Scholar
LUMSDEN, R. D. & BYRAM, J. III (1967). The ultrastructure of cestode muscle. Journal of Parasitology 53, 326–342.CrossRefGoogle Scholar
LUMSDEN, R. D. & FOOR, W. E. (1968). Electron microscopy of schistosome cercarial muscle. Journal of Parasitology 54, 780–794.CrossRefGoogle Scholar
LUMSDEN, R. D. & HILDRETH, M. B. (1983). The fine structure of adult tapeworms. In Biology of the Eucestoda, Vol. 1 (ed. Arme, C. & Pappas, P. W.), pp. 177–233. Academic Press Inc., London.
LUMSDEN, R. D. & SPECIAN, R. D. (1980). The morphology, histology, and fine structure of the adult stage of the cyclophyllidean tapeworm Hymenolepis diminuta. In Biology of the Tapeworm, Hymenolepis diminuta (ed. Arai, H. P.), pp. 157–280. Academic Press, New York and London.CrossRef
MacGREGOR, A. N. & SHORE, S. J. (1990). Immunocytochemistry of cytoskeletal proteins in adult Schistosoma mansoni. International Journal for Parasitology 20, 279–284.CrossRefGoogle Scholar
MacRAE, E. K. (1963). Observations on the fine structure of pharyngeal muscle in the planarian Dugesia tigrina. Journal of Cell Biology 18, 651–662.CrossRefGoogle Scholar
MacRAE, E. K. (1965). The fine structure of muscle in a marine turbellarian. Zeitschrift für Zellforschung und Mikroskopische Anatomie 68, 348–362.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
MAIR, G. R., MAULE, A. G., SHAW, C., JOHNSTON, C. F. & HALTON, D. W. (1998). Gross anatomy of the muscle systems of Fasciola hepatica as visualized by phalloidin-fluorescence and confocal microscopy. Parasitology 117, 75–82.CrossRefGoogle Scholar
MATSUMOTO, Y., PERRY, G., LEVINE, R. J. C., BLANTON, R., MAHMOUD, A. A. F. & AIKAWA, M. (1988). Paramyosin and actin in schistosomal teguments. Nature, London 333, 76–78.CrossRefGoogle Scholar
MILLER, C. L., DAY, T. A., BENNETT, J. L. & PAX, R. A. (1996). Schistosoma mansoni: L-glutamate-induced contractions in isolated muscle fibers; evidence for a glutamate transporter. Experimental Parasitology 84, 410–419.CrossRefGoogle Scholar
MONEYPENNY, C. G., KRESHCHENKO, N., MOFFETT, C. L., HALTON, D. W., DAY, T. A. & MAULE, A. G. (2001). Physiological effects of FMRFamide-related peptides and classical transmitters on dispersed muscle fibres of the turbellarian, Procerodes littoralis. Parasitology 122, 447–455.CrossRefGoogle Scholar
MORACZEWSKI, J. (1981). Fine structure of some Catenulida (Turbellaria, Archoophora). Zoologica Poloniae 28, 367–415.Google Scholar
MORITA, M. (1965). Electron microscopic studies on planaria. I. Fine structure of muscle fiber in the head of the planarian Dugesia dorotocephala. Journal of Ultrastructure Research 13, 383–395.Google Scholar
MUHLSCHLEGEL, F., SYGULLA, L., FROSCH, P., MASSETTI, P. & FROSCH, M. (1993). Paramyosin of Echinococcus granulosus: cDNA sequence and characterisation of a tegumental antigen. Parasitology Research 79, 660–666.CrossRefGoogle Scholar
MURAKOMO, M., USHIKI, T., ABE, K., MATSUMARA, K., SHINNO, Y. & KOYANAGI, T. (1995). Three-dimensional arrangement of collagen and elastin fibers in the human urinary bladder: a scanning electron microscopic study. Journal of Urology 154, 251–256.CrossRefGoogle Scholar
NEWPORT, G. R., HARRISON, R. A., McKERROW, J., TARR, P., KALLESTAD, J. & AGABIAN, N. (1987). Molecular cloning of Schistosoma mansoni myosin. Molecular and Biochemical Parasitology 26, 29–38.CrossRefGoogle Scholar
NORDWIG, A. & HAYDUK, U. (1969). Invertebrate collagens: isolation, characterization and phylogenetic aspects. Journal of Molecular Biology 44, 161–172.CrossRefGoogle Scholar
OLIVEIRA, G. C. & KEMP, W. M. (1995). Cloning of two actin genes from Schistosoma mansoni. Molecular and Biochemical Parasitology 75, 119–122.CrossRefGoogle Scholar
PAASONEN, M. K. & VARTIAINEN, A. (1958). Pharmacological studies on the body wall musculature of cat tapeworm (Taenia taeniaeformis). Acta Pharmacologica et Toxicologica 15, 29–36.CrossRefGoogle Scholar
PASCOLINI, R., PANARA, F., DI ROSA, I., FAGOTTI, A. & LORVIK, S. (1992 a). Characterization and fine-structural localization of actin- and fibronectin-like proteins in planaria (Dugesia lugubris s.l.). Cell and Tissue Research 267, 499–506.Google Scholar
PASCOLINI, R., DI ROSA, I., FAGOTTI, A., PANARA, F. & GABBIANI, G. (1992 b). The mammalian anti-α-smooth muscle actin monoclonal antibody recognizes an α-actin-like protein in planaria (Dugesia lugubris s.l.). Differentiation 51, 177–186.Google Scholar
PEDERSEN, K. J. (1972). Studies on regeneration blastemas of the planarian Dugesia tigrina with special reference to differentiation of the muscle-connective tissue filament system. Wilhelm Roux' Archiv fur Entwicklungsmechanik der Organismen 169, 134–169.CrossRefGoogle Scholar
REES, F. G. (1975). The arrangement and ultrastructure of the musculature, nerves and epidermis, in the tail of the cercaria of Cryptocotyle lingua (Creplin) from Littorina littorea (L.). Proceedings of the Royal Society of London, B 190, 165–186.CrossRefGoogle Scholar
REGER, J. F. (1976). Studies on the fine structure of cercarial tail muscle of Schistosoma sp. (Trematoda). Journal of Ultrastructure Research 57, 77–86.CrossRefGoogle Scholar
REISSIG, M. & COLUCCI, A. V. (1968). Localization of glycogen in the cestode, Hymenolepis diminuta. Journal of Cell Biology 39, 754–763.CrossRefGoogle Scholar
RIEGER, R., SALVENMOSER, W., LEGNITI, A., REINDL, S., ADAM, H., SIMONSBERGER, P. & TYLER, S. (1991 a). Organization and differentiation of the body-wall musculature in Macrostomum (Turbellaria, Macrostomidae). Hydrobiologia 227, 119–129.Google Scholar
RIEGER, R. M., SALVENNOSER, W., LEGNITI, A. & TYLER, S. (1994). Phalloidin-rhodamine preparations of Macrostomum hystricinum marinum (Platyhelminthes): morphology and postembryonic development of the musculature. Zoomorphology 114, 133–147.CrossRefGoogle Scholar
RIEGER, R. M., TYLER, S., SMITH, J. P. S. III & RIEGER, G. E. (1991 b). Platyhelminthes: Turbellaria. In Microscopic Anatomy of Invertebrates, Vol. 3 (ed. Harrison, F. W. & Bogitsh, B. J.), pp. 7–140. Wiley-Liss, Inc., New York.
SCHMIDT, J., BODOR, O., GOHR, L. & KUNZ, W. (1996). Paramyosin isoforms of Schistosoma mansoni are phosphorylated and localized in a large variety of muscle types. Parasitology 112, 459–467.CrossRefGoogle Scholar
SILK, M. H. & SPENCE, I. M. (1969). Ultrastructural studies of the blood fluke-Schistosoma mansoni. II. The musculature. South African Journal of Medical Science 34, 11–20.Google Scholar
STITT, A. W., FAIRWEATHER, I., TRUDGETT, A. G., JOHNSTON, C. F. & ANDERSON, S. M. L. (1992). Localisation of actin in the liver fluke, Fasciola hepatica. Parasitology Research 78, 96–102.CrossRefGoogle Scholar
TEMBE, E. A., HOLDEN-DYE, L., SMITH, S. W. G., JACQUES, P. A. M. & WALKER, R. J. (1993). Pharmacological profile of the 5-hyroxytryptamine receptor of Fasciola hepatica body wall muscle. Parasitology 106, 67–73.CrossRefGoogle Scholar
TOMOSKY-SYKES, T. K., MUELLER, J. F. & BUEDING, E. (1977). Effects of putative neurotransmitters on the motor activity of Spirometra mansonoides. Journal of Parasitology 63, 492–494.CrossRefGoogle Scholar
TORRE-BLANCO, A. & TOLEDO, I. (1981). The isolation, purification, and characterization of the collagen of Cysticercus cellulosae. Journal of Biological Chemistry 256, 5926–5930.Google Scholar
TYLER, S. & HYRA, G. S. (1998). Patterns of musculature as taxonomic characters for the Turbellaria Acoela. Hydrobiologia 383, 51–59.CrossRefGoogle Scholar
TYLER, S. & RIEGER, R. M. (1999). Functional morphology of musculature in the acoelomate worm, Convoluta pulchra (Platyhelminthes). Zoomorphology 119, 127–141.CrossRefGoogle Scholar
VARGAS-PARADA, L. & LACLETTE, J. P. (2003). Gene structure of Taenia solium paramyosin. Parasitology Research 89, 375–378.Google Scholar
VENTURINI, G., STOCCHI, F., MARGOTTA, V., RUGGIERI, S., BRAVI, D., BELLANTUONO, P. & PALLADINI, G. (1989). A pharmacological study of dopaminergic receptors in planaria. Neuropharmacology 28, 1377–1382.CrossRefGoogle Scholar
WAHLBERG, M. H. (1997). Three main patterns in the expression of six actin genes in the plerocercoid and adult Diphyllobothrium dendriticum tapeworm (Cestoda). Molecular and Biochemical Parasitology 86, 199–209.CrossRefGoogle Scholar
WAHLBERG, M. H. (1998). The distribution of F-actin during the development of Diphyllobothrium dendriticum (Cestoda). Cell and Tissue Research 291, 561–570.CrossRefGoogle Scholar
WAHLBERG, M. H. & JOHNSON, M. S. (1997). Isolation and characterization of five actin cDNAs from the cestode Diphyllobothrium dendriticum: a phylogenetic study of the multigene family. Journal of Molecular Evolution 44, 159–168.CrossRefGoogle Scholar
WAHLBERG, M. H., KARLSTEDT, K. A. & PAATERO, G. I. L. (1994). Cloning, sequencing and characterization of an actin cDNA in Diphyllobothrium dendriticum (Cestoda). Molecular and Biochemical Parasitology 65, 357–360.CrossRefGoogle Scholar
WARD, S. M., ALLEN, J. M. & McKERR, G. (1986). Neuromuscular physiology of Grillotia erinaceus metacestodes (Cestoda: Trypanorhyncha) in vitro. Parasitology 93, 121–132.CrossRefGoogle Scholar
WEBB, R. A. (1977). The organization and fine structure of the muscles of the scolex of the cysticercoid of Hymenolepis microstoma. Journal of Morphology 154, 339–356.CrossRefGoogle Scholar
WEBB, R. A. (1987). Innervation of muscle in the cestode Hymenolepis microstoma. Canadian Journal of Zoology 65, 928–935.CrossRefGoogle Scholar
WESTON, D., SCHMITZ, J., KEMP, W. M. & KUNZ, W. (1993). Cloning and sequencimg of a complete myosin heavy chain cDNA from Schistosoma mansoni. Molecular and Biochemical Parasitology 58, 161–164.CrossRefGoogle Scholar
WILLMS, K., ROBERT, L. & CARO, J. A. (2003). Ultrastructure of smooth muscle, gap junctions and glycogen distribution in Taenia solium tapeworms from experimentally infected hamsters. Parasitology Research 89, 308–316.Google Scholar
WILSON, R. A. (1969). Fine structure and organization of the musculature in the miracidium of Fasciola hepatica. Journal of Parasitology 55, 1153–1161.CrossRefGoogle Scholar
XU, H., MILLER, S., VAN KEULEN, H., WAWRZYNSKI, M. R., REKOSH, D. M. & LOVERDE, P. T. (1989). Schistosoma mansoni tropomyosin: cDNA characterization, sequence, expression, and gene product localization. Experimental Parasitology 69, 373–392.CrossRefGoogle Scholar