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Antigen localization and the induction of resistance in mice vaccinated with irradiated cercariae of Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

A. P. Mountford
Affiliation:
Department of Biology, University of York, York YOl 5DD
P. S. Coulson
Affiliation:
Department of Biology, University of York, York YOl 5DD
R. A. Wilson
Affiliation:
Department of Biology, University of York, York YOl 5DD

Summary

The fate of 75Se-labelled parasites and their released pre-synthesized macromolecules has been followed in three murine infection models. Parasite numbers in specific tissues were determined by autoradiography, and released material was estimated by gamma-counting of tissues, with adjustment for the presence of parasite-associated radiolabel. Marked differences were found between the three models. The pattern of migration of normal schistosomula was similar to that previously reported. In addition we have described the transit of parasites through the lymph nodes draining the infection site. Significant quantities of released material were detected in the skin, draining lymph nodes, bloodstream and liver. The circulating material was of parasite origin, macromolecular, and hence potentially antigenic. In comparison to the normal infection, radiation-attenuated parasites (inducing a high level of resistance to challenge) persisted in the skin, draining lymph nodes and lungs, releasing a proportionally greater amount of material in the nodes. In mice exposed to attenuated parasites and treated with the compound ROl1–3128 at 24 h (inducing a low level of resistance) there was an early death and rapid clearance of the parasites whilst still in the skin. This situation resulted in the highest levels of released material in the skin, bloodstream and liver, but negligible levels in the draining lymph nodes. We suggest that the persistence of radiation-attenuated parasites in the skin and draining lymph nodes, together with the prolonged release of antigen in the latter site, compared to the normal situation, are major factors in the induction of resistance.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

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References

REFERENCES

Ada, G. L., Nossal, G. J. V. & Pye, J. (1964). Antigens in immunity. III. Distribution of iodinated antigens following injection into rats via the hind footpads. Australian Journal of Experimental Biology and Medical Science 42, 295310.CrossRefGoogle ScholarPubMed
Aitken, R., Coulson, P. S., Dixon, B. & Wilson, R. A. (1987). Radiation-resistant acquired immunity of vaccinated mice to Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 37, 570–7.Google Scholar
Bickle, Q. D. (1982). Studies on the relationship between the survival of Schistosoma mansoni larvae in mice and the degree of resistance produced. Parasitology 84, 111–22.Google Scholar
Bickle, Q. D. & Andrews, B. J. (1985). Resistance following drug-attenuation (RO11–3128 or Oxamniquine) of early Schistosoma mansoni infections in mice. Parasitology 90, 325–38.CrossRefGoogle ScholarPubMed
Christensen, N. O. (1977). A method for the in vivo labelling of Schistosoma mansoni and S. intercalatum cercariae with radioselenium. Zeitschrift für Parasitenkunde 54, 275–88.Google Scholar
Crabtree, J. E. & Wilson, R. A. (1986). The role of pulmonary cellular reactions in the resistance of vaccinated mice to Schistosoma mansoni. Parasite Immunology 8, 265–85.Google Scholar
Dean, D. A. (1983). A review of Schistosoma and related genera: Acquired resistance in mice. Experimental Parasitology 55, 1104.Google Scholar
Fraker, P. J. & Spek, J. C. (1978). Protein and cell membrane iodination with sparingly soluble chloramide 1,3,4,6-tetrachloro -3, 6-diphenylglycouril. Biochemical Biophysical Research Communications 80, 849–57.Google Scholar
Georgi, J. R. (1982). Schistosoma mansoni: quantification of skin penetration and early migration by differential external radioassay and autoradiography. Parasitology 84, 263–81.Google Scholar
Hudson, L. & Hay, F. C. (1980). Practical Immunology 2nd ed. pp. 107–6. Oxford: Blackwell Scientific Publications.Google Scholar
Humphrey, J. H. (1982). The fate of antigens. In Clinical Aspects of Immunology, vol. 1, 4th ed. (ed. Lachmann, P. J. and Peters, D. K.), pp. 161–86. Oxford: Blackwell Scientific Publications.Google Scholar
James, S. L., Labine, M. & Sher, A. (1981). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. I. Analysis of the antibody and T lymphocyte responses in mouse strains developing differing levels of immunity. Cellular Immunology 65, 7583.CrossRefGoogle Scholar
Mangold, B. L. & Dean, D. A. (1983). Autoradiographic analysis of Schistosoma mansoni migration from skin to lungs in naive mice. Evidence that most attrition occurs after the skin phase. American Journal of Tropical Medicine and Hygiene 32, 785–9.Google Scholar
Mangold, B. L. & Dean, D. A. (1984). The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host-parasite contact in relation to the induction of resistance in mice. Parasitology 88, 249–66.CrossRefGoogle Scholar
Mastin, A. J., Bickle, Q. D. & Wilson, R. A. (1983). Schistosoma mansoni: migration and attrition of irradiated and challenge schistosomula in the mouse. Parasitology 87, 87102.CrossRefGoogle ScholarPubMed
Mastin, A. J., Bickle, Q. D. & Wilson, R. A. (1985). An ultrastructural examination of irradiated, immunizing schistosomula of Schistosoma mansoni during their extended stay in the lungs. Parasitology 81, 101–10.CrossRefGoogle Scholar
Nagai, Y., Gazzinelli, G., de Moraes, G. W. G. & Pellegrino, J. (1977). Protein synthesis during cercaria-schistosomulum transformation and early development of the Schistosoma mansoni larvae. Comparative Biochemistry and Physiology 578, 2730.Google Scholar
Pearce, E. J., Basch, J. & Sher, A. (1986). Evidence that the reduced surface antigenicity of developing Schistosoma mansoni schistosomula is due to antigen shedding rather than host molecule acquisition. Parasite Immunology 8, 7994.Google Scholar
Rogoff, T. M. & Lipsky, P. E. (1981). Role of the Kupffer cells in local and systemic immune responses. Gastroenterology 8, 854–60.CrossRefGoogle Scholar
Samuelson, J. C. & Caulfield, J. P. (1982). Loss of covalently labelled glycoproteins and glycolipids from the surface of newly transformed schistosomula of Schistosoma mansoni. Journal of Cell Biology 94, 363–9.CrossRefGoogle ScholarPubMed
Sher, A., Hieny, S., James, S. L. & Asofsky, R. (1982). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. II Analysis of immunity in hosts deficient in T lymphocytes, B lymphocytes or complement. Journal of Immunology 128, 1880–4.CrossRefGoogle ScholarPubMed
Simpson, A. J. G., Hackett, F., Walker, T., De Rossi, R. & Smithers, S. R. (1985). Antibody responses against schistosomulum surface antigens and protective immunity following immunization with highly irradiated cercariae of Schistosoma mansoni. Parasite Immunology 7, 133–52.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, R. J. (1965). Infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695700.CrossRefGoogle ScholarPubMed
Streilein, W. J., Stein-Streilein, J. & Head, J. (1986). Regional specialization in antigen presentation. In The Reticuloendothelial System; A Comprehensive Treatise, vol. 9, Hypersensitivity, (ed. Phillips, S. M. and Escobar, M. R.), pp. 3793. New York and London: Plenum.CrossRefGoogle Scholar
Wheater, P. R. & Wilson, R. A. (1979). Schistosoma mansoni: a histological study of migration in the laboratory mouse. Parasitology 75, 4962.CrossRefGoogle Scholar
Wilson, R. A. & Coulson, P. S. (1986). Schistosoma mansoni: dynamics of migration through the vascular system of the mouse. Parasitology 92, 83100.Google Scholar
Wilson, R. A., Coulson, P. S. & Dixon, B. (1986). Migration of the schistosomula of Schistosoma mansoni in mice vaccinated with radiation attenuated cercariae, and normal mice: an attempt to identify the timing and site of parasite death. Parasitology 92, 101–16.Google Scholar
Wilson, R. A., Coulson, P. S. & McHugh, S. M. (1983). A significant part of the ‘concomitant immunity’ of mice to Schistomosa mansoni is a consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595601.CrossRefGoogle Scholar