Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T00:28:21.074Z Has data issue: false hasContentIssue false

Serum from CBA/Ca mice vaccinated with irradiated cercariae of Schistosoma mansoni protects naive recipients through the recruitment of cutaneous effector cells

Published online by Cambridge University Press:  06 April 2009

Diane J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
S. R. Smithers
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA

Summary

Passive transfer experiments showed that 76% of the resistance induced in CBA/Ca mice by exposure to radiation-attenuated cercariae of Schistosoma mansoni could be transferred to naive recipients by administration of donor serum. The level of protection achieved depended on the volume of serum administered and immunity was demonstrated most consistently with serum harvested from thrice vaccinated donors. The serum was twice as effective when given to the recipients at the time of cercarial challenge as compared to administration 5 days after challenge, a result which indicates that serum-dependent challenge elimination is probably accomplished in the cutaneous tissues. This view was confirmed by the observation that passive protection could be ablated by administration of a monoclonal antibody which we have shown elsewhere to deplete the cutaneous inflammatory reaction to cercarial penetration. Histopathological studies revealed that vaccine serum induced subdermal inflammatory reactions in challenged recipient mice which were identical both in induration and kinetics to those seen in conventionally vaccinated individuals; on days 4 and 5 post-challenge, the reactions comprised 60% mononuclear cells and 40% eosinophils. Challenge larvae, which had transformed from skin-stage to lung-stage parasites, became trapped within such reactions and eventually showed generalized vacuolation consistent with the onset of damage. Some foci were seen to contain degenerated leucocytes, free eosinophil granules and debris which is thought to represent the remnants of dead parasites. Small focal reactions were identified on occasion in naive challenged mice and in recipients of normal mouse serum, but these reactions comprised predominantly mononuclear cells and were rarely seen to encompass challenge parasites. These data show that serum-transferred resistance in the vaccinated CBA/Ca mouse model involves the induction of a cutaneous inflammatory response in the recipients.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

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

REFERENCES

Anwar, A. R. E. & Kay, A. B. (1978). Enhancement of human eosinophil complement receptors by pharmacologic mediators. Journal of Immunology 121, 1245–50.CrossRefGoogle ScholarPubMed
Cardella, C. J., Davies, P. & Allison, A. C. (1974). Immune complexes induce selective release of lysosomal hydrolases from macrophages. Nature, London 247, 46–8.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, 8996.CrossRefGoogle ScholarPubMed
Fearon, D. T. & Wong, W. W. (1983). Complement ligand-receptor interactions that mediate biological responses. In Annual Reviews of Immunology, vol. 1 (ed. Paul, W. E.), p. 243. Palo Alto, California: Annual Reviews Inc.Google Scholar
Ford, M. J., Bickle, Q. D., Taylor, M. G. & 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
James, S. L. & Cheever, A. W. (1985). Comparison of immune responses between high and low responder strains of mice in the concomitant immunity and vaccine models of resistance to Schistosoma mansoni. Parasitology 91, 301–15.CrossRefGoogle ScholarPubMed
James, S. L., Correa-Oliviera, R. & Leonard, E. J. (1984). Defective immunity to Schistosoma mansoni in P strain mice. II. Analysis of cellular responses. Journal of Immunology 133, 1587–93.CrossRefGoogle Scholar
James, S. L., Deblois, L. A., Al-Zamel, F., Glaren, J. & Langhorne, J. (1986). Defective vaccine-induced resistance to Schistosoma mansoni in P strain mice. III. Specificity of the associated defect in cell-mediated immunity. Journal of Immunology 127, 3959–67.CrossRefGoogle Scholar
James, S. L. & Sher, A. (1983). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. III. Identification of a mouse strain, P/N, that fails to respond to vaccination. Parasite Immunology 5, 567–75.CrossRefGoogle Scholar
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
Kay, A. B. (1970). Studies on eosinophil leucocyte migration. II. Factors preferentially chemotactic for eosinophils and neutrophils generated from guinea-pig serum by antigen-antibody complexes. Clinical Experimental Immunology 7, 723–37.Google Scholar
Lendrum, A. C. (1944). The staining of eosinophil polymorphs and enterochromaffin cells in histological sections. Journal of Pathology and Bacteriology 56, 441.CrossRefGoogle Scholar
Lopez, A. F., Strath, M. & Sanderson, C. J. (1984). Differentiation antigens on mouse eosinophils and neutrophils identified by monoclonal antibodies. British Journal of Haematology 57, 489–94.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 ScholarPubMed
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
McLaren, D. J. (1980). Schistosoma mansoni: the parasite surface in relation to host immunity. In Tropical Medicine Research Studies, vol. 1 (ed. Brown, K. N.), pp. 1229. Chichester: John Wiley/Research Studies Press.Google Scholar
McLaren, D. J. & James, S. L. (1985). Ultrastructural studies of the killing of schistosomula of Schistosoma mansoni by activated macrophages in vitro. Parasite Immunology 7, 315–31.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, 2944.CrossRefGoogle ScholarPubMed
McLaren, D. J., Peterson, C. G. B. & Venge, P. (1985). Schistosoma mansoni: further studies of the interaction between schistosomula and granulocyte-derived cationic proteins in vitro. Parasitology 88, 491503.CrossRefGoogle Scholar
McLaren, D. J. & Ramalho-Pinto, F. J. (1979). Eosinophil-mediated killing of schistosomula of Schistosoma mansoni in vitro: synergistic effect of antibody and complement. Journal of Immunology 123, 1431–8.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, 19.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. and Simpson, A. J. G.), pp. 233–63. London: Academic Press.Google Scholar
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 deplgtes cutaneous effector cells. Parasite Immunology 9, 667–82.CrossRefGoogle ScholarPubMed
Miller, K. L. & Smithers, S. R. (1980). Schistosoma mansoni: the attrition of a challenge infection in mice immunised with highly irradiated live cercariae. Experimental Parasitology 50, 212–21.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, 2531.CrossRefGoogle ScholarPubMed
Pestel, J., Joseph, M., Dessaint, J. P. & Capron, A. (1981). Macrophage triggering by aggregated immunoglobulins. 1. Delayed effects of IgG aggregates on immune complexes. Journal of Immunology 126, 1887–91.CrossRefGoogle ScholarPubMed
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, 695700.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 the vaccinated CBA/Ca mouse. Parasitology 96, 6384.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed