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Schistosoma mansoni: evidence that site-dependent host responses determine when and where vaccine immunity is expressed in different rodent species

Published online by Cambridge University Press:  06 April 2009

V. S. Delgado  and
D. J. McLaren
V. S. Delgado
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 IAA
D. J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 IAA
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Summary

Laboratory rodents vaccinated with highly irradiated cercariae of Schistosoma mansoni develop significant levels of specific acquired resistance yet effect challenge elimination in different organs. Mice and guinea-pigs are at opposite ends of the spectrum in this respect since, in our hands, vaccinated mice kill challenge parasites in the skin whereas vaccinated guinea-pigs kill challenge parasites predominantly in the liver. To determine whether this phenomenon is host-dependent (site) or parasite-dependent (stage), we have transferred worms harvested from mice or guinea-pigs into vaccinated recipient guinea-pigs. The results show that mouse-derived 5-day lung worms and 9-day liver worms that are essentially refractory to vaccine resistance in mice are indeed susceptible to vaccine resistance in guinea-pigs. Identical levels of susceptibility were recorded for lung-stage larvae introduced via the foot vein so as to experience lung and liver mechanisms, or via the mesenteric vein to bypass the lung, thereby confirming that vaccine resistance in guinea-pigs operates in the liver. Mouse worms and guinea-pig worms exhibited equivalent levels of susceptibility at all stages of development. Thirteen-day-old larvae from either donor species were on the border-line of vulnerability, while 20-day-old worms were totally refractory to vaccine immunity in guinea-pigs. These data show that vaccine immunity in different rodent species is a site-dependent, rather than a stage-dependent phenomenon. There is, however, an upper age limit of schistosome vulnerability which is common to worms harvested from different donor species.

Keywords

Schistosoma mansoniirradiated vaccine modelguinea-pigsmicesite-dependent immunity
Type
Research Article
Information
Parasitology , Volume 100 , Issue 1 , February 1990 , pp. 57 - 63
Copyright
Copyright © Cambridge University Press 1990

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References

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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Dean, D. A., Mangold, B. L., Georgi, J. R. & Jacobson, R. H. (1984). Comparison of Schistosoma mansoni migration patterns in normal and irradiated cercaria-immunized mice by means of autoradiographic analysis. Evidence that worm elimination occurs after the skin phase in immunized mice. American Journal of Tropical Medicine and Hygiene 33, 89–96.CrossRefGoogle ScholarPubMed
Delgado, V. & McLaren, D. J. (1989). Contribution of IgG1 and radio-resistant cells to immune expression in guinea pigs vaccinated with radiation-attenuated cercariae of Schistosoma mansoni. International Journal for Parasitology (in the Press).Google Scholar
Delgado, V. & McLaren, D. J. (1990). Evidence that radio-sensitive cells are central to skin-phase protective immunity in CBA/Ca mice vaccinated with radiation-attenuated cercariae of Schistosoma mansoni as well as in naive mice protected with vaccine serum. Parasitology 100, 45–56.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D., Taylor, M. J. & Andrews, B. J. (1984). Passive transfer of resistance and the site of immune-dependent elimination of the challenge infection in rats vaccinated with highly irradiated cercariae of Schistosoma mansoni. Parasitology 89, 461–82.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D. & Taylor, M. J. (1987). Immunity to Schistosoma mansoni in congenitally athymic, irradiated and mast cell depleted rats. Parasitology 94, 313–26.CrossRefGoogle ScholarPubMed
Kamiya, H., Smithers, S. R. & McLaren, D. J. (1987). Schistosoma mansoni: autoradiographic tracking studies of isotopically-labelled challenge parasites in naive and vaccinated CBA/Ca mice. Parasite Immunology 9 515–29.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1983). Autoradiographic analysis of Schistosoma mansoni migration from skin to lungs in naive mice. Evidence that most of the attrition occurs after the skin phase. American Journal of Tropical Medicine and Hygiene 32, 785–9.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1986). Passive transfer with serum and IgG antibodies of irradiated cercariae-induced resistance against Schistosoma mansoni in mice. Journal of Immunology 136, 2644–8.CrossRefGoogle Scholar
Mangold, B. L., Dean, D. A., Coulson, P. S. & Wilson, R. A. (1986). Site requirements and kinetics of immune-dependent elimination of intravascularly administered lung stage schistosomula in mice immunized with highly irradiated cercariae of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 35, 332–40.CrossRefGoogle ScholarPubMed
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, 87–102.CrossRefGoogle ScholarPubMed
McLaren, D. J., Delgado, V., Gordon, J. R. & Rogers, M. V. (1990). Schistosoma mansoni: analysis of the humoral and cellular basis of resistance in guinea-pigs vaccinated with radiation-attenuated cercariae. Parasitology 100, 35–44.CrossRefGoogle ScholarPubMed
McLaren, D. J., Pearce, E. J. & Smithers, S. R. (1985). Site potential for challenge attrition in mice, rats and guinea-pigs vaccinated with irradiated cercariae of Schistosoma mansoni. Parasite Immunology 7, 29–44.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Rogers, M. V. (1986). Schistosoma mansoni: liver phase challenge attrition is a stage-dependent phenomenon in guinea pigs vaccinated with highly irradiated cercariae. Parasite Immunology 8, 307–18.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Smithers, S. R. (1985). Schistosoma mansoni: challenge attrition during the lung phase of migration in vaccinated and serum-protected rats. Experimental Parasitology 60, 1–9.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Smithers, S. R. (1987). The immune response to schistosomes in experimental hosts. In The Biology of Schistosomes (ed. Rollinson, D. & Simpson, A. J. G.), pp. 233–63. London: Academic Press.Google Scholar
McLaren, D. J. & Smithers, S. R. (1988). Serum from CBA/Ca mice vaccinated with irradiated cercariae of Schistosoma mansoni protects naive recipients through the recruitment of cutaneous effector cells. Parasitology 97, 287–309.Google ScholarPubMed
McLaren, D. J., Strath, M. & Smithers, S. R. (1987). Schistosoma mansoni: evidence that immunity in vaccinated and chronically infected CBA/Ca mice is sensitive to treatment with a monoclonal antibody that depletes cutaneous effector cells. Parasite Immunology 9, 667–82.CrossRefGoogle ScholarPubMed
Miller, K. L., Smithers, S. R. & Sher, A. (1981). The response of mice immune to Schistosoma mansoni to a challenge infection which bypasses the skin: evidence for two mechanisms of immunity. Parasite Immunology 3, 25–31.CrossRefGoogle ScholarPubMed
Miller, P. & Wilson, R. A. (1980). Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 80, 267–80.CrossRefGoogle Scholar
Pearce, E. J. & McLaren, D. J. (1983). Schistosoma mansoni: in vivo and in vitro studies of immunity using the guinea-pig model. Parasitology 87, 465–79.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Gammage, K. (1980). The recovery of Schistosoma mansoni from the skin, lungs and hepatic portal system of naive mice and mice previously exposed to S. mansoni. Evidence for two phases of parasite attrition in immune mice. Parasitology 80, 289–300.CrossRefGoogle Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Vignali, D. A. A., Bickle, Q. D. & Taylor, M. G. (1988). Studies on immunity to Schistosoma mansoni in vivo: whole-body irradiation has no effect on vaccine-induced resistance in mice. Parasitology 96, 49–61.CrossRefGoogle ScholarPubMed
Vignali, D. A. A., Klaus, S. N., Bickle, Q. D. & Taylor, M. G. (1989). Histological examination of the cellular reactions around schistosomula of Schistosoma mansoni in the lungs of sublethally irradiated and unirradiated, immune and control rats. Parasitology 98, 57–65.CrossRefGoogle ScholarPubMed
Ward, R. E. M. & McLaren, D. J. (1988). Schistosoma mansoni: evidence that eosinophils and/or macrophages contribute to skin-phase challenge attrition in vaccinated CBA/Ca mice. Parasitology 96, 63–84.CrossRefGoogle ScholarPubMed
Ward, R. E. M. & McLaren, D. J. (1989). Schistosoma mansoni: migration and attrition of challenge parasites in naive rats and rats protected with vaccine serum. Parasite Immunology 11, 125–46.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S. & Dixon, B. (1986). Migration of 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.CrossRefGoogle ScholarPubMed