Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T10:12:04.789Z Has data issue: false hasContentIssue false

Schistosoma mansoni: a comparative study of schistosomula transformed mechanically and by skin penetration. Electrophysiological responses to a wide range of substances

Published online by Cambridge University Press:  06 April 2009

D. P. Thompson
Affiliation:
Departments of Pharmacology and Toxicology, and Zoology, and Neuroscience Program, Michigan State University, East Lansing, Michigan 48824
R. A. Pax
Affiliation:
Departments of Pharmacology and Toxicology, and Zoology, and Neuroscience Program, Michigan State University, East Lansing, Michigan 48824
J. L. Bennett
Affiliation:
Departments of Pharmacology and Toxicology, and Zoology, and Neuroscience Program, Michigan State University, East Lansing, Michigan 48824

Summary

Volume conducted potentials were recorded from schistosomula of Schistosoma mansoni transformed mechanically (MS) and by skin penetration (SS). The spontaneous electrical activity recorded consisted of bi and triphasic transients ranging from 20 to 200 μV in amplitude and 10 to 300 msec in duration. Low amplitude potentials occurred at a much greater frequency than large amplitude potentials, which appeared to correlate with peristaltic-like contractions of the schistosomulum's musculature. Electrical activity in the schistosomulum was highly sensitive to a number of agents believed to affect metabolic pathways, the neuromuscular system or the host/parasite interface of adult schistosomes. Among the most reactive substances were potassium antimony tartrate, eserine, poly-L-arginine and potassium cyanide. Over a wide range of experimental treatments, electrophysiological responses in schistosomula transformed from cercariae by mechanical decaudation and skin penetration were remarkably similar, supporting the notion that MS are suitable material for in vitro immunochemical, biochemical and physiological study. Some treatments, however, were more or less effective in altering electrophysiological activity and motility in the schistosomulum than in adult S. mansoni. This suggests that significant physiological alterations may occur during development from skin stage to adult parasites concomitant with immunochemical and morphological changes already known to occur.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bennett, J. L., Bueding, E., Timms, A. R. & Engstrom, R. (1969). Occurrence and levels of 5-HT i. Schistosoma mansoni. Molecular Pharmacology 5, 542–5.Google ScholarPubMed
Bickle, Q. D. & Ford, M. J. (1982). Studies on the surface antigenicity and susceptibility to antibody-dependent killing of developing schistosomula using sera from chronically infected mice and mice vaccinated with irradiated cercariae. Journal of Immunology 128, 2101–6.CrossRefGoogle ScholarPubMed
Brink, L. H., Mclaren, D. J. & Smithers, S. R. (1977). Schistosoma mansoni: A comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74, 7386.Google Scholar
Brown, M. C., Koura, M., Bell, D. R. & Giles, H. M. (1973). An in vitro activity monitor for schistosomes: a preliminary report. Annals of Tropical Medicine and Parasitology 76, 369–70.CrossRefGoogle Scholar
Bruce, J. I., Pezzlo, F., McCarthy, J. E. & Yajima, Y. (1970). Migration of Schistosoma mansoni through mouse tissue. Ultrastructure of host tissue and integument of migrating larva following cercarial penetration. American Journal of Tropical Medicine and Hygiene 19, 959–81.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Wassom, D. L., Gleich, G. J., Loegering, P. A. & David, J. R. (1979). Damage to schistosomula of Schistosoina mansoni induced directly by eosinophil major basic protein. Journal of Immunology 122, 221–9.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1968). Death of schistosome cercariac during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology 58, 111–28.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1972). The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 7998.Google Scholar
Coles, G. C. (1972). Carbohydrate metabolism of larval Schistosoma mansoni. International Journal for Parasitology 2, 341–52.Google Scholar
Colley, D. G. & Wickel, S. K. (1974). Schistosoma mansoni: simplified method for the production of schistosomules. Experimental Parasitology 35, 44–5.CrossRefGoogle ScholarPubMed
Cousin, C. E., Stirewalt, M. A. & Dorsey, C. H. (1981). Schistosoma mansoni: ultrastructure of early transformation of skin- and shear-pressure-derived schistosomules. Experimental Parasitology 51, 341–65.Google Scholar
Dean, D. A. (1977). Decreased binding of cytotoxic antibody by developing Schistosoma mansoni. Evidence for a surface change independent of host antigen adsorption and membrane turnover. Journal of Parasitology 63, 418–26.Google Scholar
Dessein, A. J., Samuelson, J. C., Butterworth, A. E., Hogan, M., Sherry, B. A., Vadas, M. A. & David, J. R. (1981). Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82, 357–74.CrossRefGoogle ScholarPubMed
Fetterer, R. H. & Pax, R. A. (1981). Na+-K+-ttransport, motility and tegumental membrane potential in adult male Schistosoma mansoni. Parasitology 82, 97109.CrossRefGoogle ScholarPubMed
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1977). Schistosoma mansoni: direct method for simultaneous recordings of the electrical and motor activity. Experimental Parasitology 43, 286–94.CrossRefGoogle ScholarPubMed
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1980). Praziquantel, potassium and 2,4-dinitrophenol: analysis of their action on the musculature of Schistosoma mansoni. European Journal of Pharmacology 64, 31–8.CrossRefGoogle ScholarPubMed
Georgi, J. R., Dean, D. A. & Mangold, B. L. (1983). Schistosoma mansoni: temporal distribution of radioselenium-labelled schistosomula in lungs of mice during the first two weeks of infection. Parasitology 86, 31–6.Google Scholar
Glauert, A. M. & Butterworth, A. E. (1977). Morphological evidence for the ability of eosinophils to damage antibody-coated schistosomula. Transactions of the Royal Society for Tropical Medicine and Hygiene 71, 392403.CrossRefGoogle ScholarPubMed
Haas, W. & Schmitt, R. (1982). Characterization of chemical stimuli for the penetration of Schistosoma mansoni cercariae. I. Effective substances, host specificity. Zeitschrift für Parasitenkunde 66, 293307.CrossRefGoogle ScholarPubMed
Hillman, G. R. & Senft, A. W. (1973). Schistosome motility measurements: response to drugs. Journal of Pharmacology and Experimental Therapeutics 185, 177–84.Google ScholarPubMed
Hockley, D. J. & McLaren, D. J. (1973). Schistosoma mansoni: Changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 1325.CrossRefGoogle ScholarPubMed
Kusel, J. R. (1972). Protein composition and protein synthesis in the surface membranes of Schistosoma mansoni. Parasitology 65, 5569.Google Scholar
McLaren, D. J., Hockley, D. J., Goldring, O. L. & Hammond, B. J. (1978). A freeze fracture study of the developing tegumental outer membrane of Schistosoma mansoni. Parasitology 76, 327–48.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Incani, R. N. (1982). Schistosoma mansoni: acquired resistance of developing schistosomula to immune attack in vitro. Experimental Parasitology 53, 285–98.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Terry, H. J. (1982). The protective role of acquired host antigens during schistosome maturation. Parasite Immunology 4, 129–48.CrossRefGoogle ScholarPubMed
Mellin, T. N., Busch, R. D., Wang, C. C. & Kath, G. (1983). Neuropharmacology of the parasitic trematode, Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 32, 106–13.Google Scholar
Moser, G., Wassom, D. L. & Sher, A. (1980). Studies of the antibody-dependent killing of schistosomula of Schistosoma mansoni employing haptenic target antigens. I. Evidence that the loss in susceptibility to immune damage undergone by developing schistosomula involves a change unrelated to the masking of host antigens by host molecules. Journal of Experimental Medicine 152, 4154.CrossRefGoogle Scholar
Murrell, K. D., Taylor, D. W., Vannier, W. E. & Dean, D. A. (1978). Schistosoma mansoni: analysis of surface membrane carbohydrates using lectins. Experimental Parasitology 46, 247–55.CrossRefGoogle ScholarPubMed
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. F., Mota-Santos, T. A., Figueiredo, E. A. & Pellegrino, J. (1974). Schistosoma mansoni: a defined system for the step-wise transformation of the cercaria to schistosomule in vitro. Experimental Parasitology 36, 360–72.Google Scholar
Rumjanek, F. D. (1982). Schistosoma mansoni: membrane lipid modulation and acquisition of resistance against immune damage. Abstracts: WHO Scientific working group on the schistosome membrane, Item 18.Google Scholar
Samuelson, J. C., Caulfield, J. P. & David, J. R. (1980). Schistosoma mansoni: post- transformational surface changes in schistosomula grown in vitro and in mice. Experimental Parasitology 50, 369–83.CrossRefGoogle ScholarPubMed
Semeyn, D. R., Pax, R. A. & Bennett, J. L. (1982). Surface electrical activity from Schistosoma mansoni: a sensitive measure of drug action. Journal of Paracitology 68, 353–62.Google Scholar
Sher, A. (1977). Immunity against Schistosoma manconi in the mouse. American Journal of Tropical Medicine and Hygiene 26, 1119.CrossRefGoogle Scholar
Smith, H. V. & Kusel, J. R. (1979). The acquisition of antigens in the intercellular substance of mouse skin by schistosomula of Schistosoma mansoni. Clinical and Experimental Immunology 36, 430–5.Google ScholarPubMed
Smithers, S. R., Terry, R. J. & Hockley, D. J. (1969). Host antigens in schistosomiasis. Proceedings of the Royal Society, B 171, 483–94.Google ScholarPubMed
Smithers, S. R. & Gammage, Y. (1980). Recovery of Schistosoma mansoni from skin, lungs and hepatic portal system of naive mice and mice previously exposed to S. mansoni. Parasitology 80, 289300.Google Scholar
Stirewalt, M. A. (1963). Cercaria vs. schistosomule (Schistosoma mansoni): absence of the pericercarial envelope in vivo and the early physiological and histological metamorphosis of the parasite. Experimental Parasitology 13, 395406.CrossRefGoogle ScholarPubMed
Tavares, C. A. P., Gazzinelli, G., Mota-Santos, T. A. & Dias Da Silva, W. (1978). Schistosoma mansoni: evidence for a role of serum factors in protecting artificially transformed schistosomula against antibody-mediated killing in vitro. Parasitology 77, 225–33.Google Scholar
Thompson, D. P., Pax, R. A. & Bennett, J. L. (1982 a). Microelectrode studies of the tegument and subtegumental compartments of male Schistosoma mansoni: an analysis of electro physiological properties. Paracitology 85, 163–78.CrossRefGoogle Scholar
Thompson, D. P., Pax, R. A. & Bennett, J. L. (1982 b). Electrophysiological studies of schistosomula of Schistosoma mansoni. Abstracts of the Fifth International Society of Parasitologists, Toronto, Canada.Google Scholar
Tomosky, T. K., Bennett, J. L. & Bueding, E. (1974). Tryptaminergic and dopaminergic responses of Schistosoma mansoni. Journal of Pharmacology and Experimental Therapeutics 190, 260–71.Google Scholar
Van Pijkeren, T. A., Tavares, C. A. P. & Gazzinelli, G. (1982). Schistosoma mansoni: ability of Con A to protect in vitro mechanically transformed schistosomula against the lethal effect of immune serum plus complement. Parasitology 84, 239–52.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Barnes, P. E. (1974). An in vitro investigation of dynamic processes occurring in the schistosome tegument, using compounds known to disrupt secretory processes. Parasitology 68, 259–70.CrossRefGoogle Scholar
Zodda, D. M. & Phillips, S. M. (1982). Monoclonal antibody-mediated protection against Schistosoma mansoni infection in mice. Journal of Immunology 129, 2326–8.CrossRefGoogle ScholarPubMed