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Radiation-attenuated schistosome vaccination – a brief historical perspective

Published online by Cambridge University Press:  30 March 2009

Q. D. BICKLE
Q. D. BICKLE*
Affiliation:
Immunology Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
*
*Tel: +0207 927 2609. Fax: 0207 323 5687/636 8739. E-mail: [email protected]
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Summary

The high level of protection which can be induced by vaccination of a range of hosts, from rodents to primates, with live radiation-attenuated schistosome larvae offers great promise for development of a human schistosome vaccine. Studies of the irradiated vaccine models benefitted from significant funding during the 1970–90s and much was learned concerning the inducers, targets and mechanisms of immunity. Less progress was made in definition of the protective antigens involved. The application of new techniques for identifying membrane and secreted antigens has recently provided new vaccine candidates and a new impetus for schistosome vaccine development. This article is intended as an overview of some of the main lessons learned from the studies of the irradiated vaccines as a backdrop to renewed interest in schistosome vaccine development.

Keywords

schistosomiasisradiation attenuationmembrane antigenssecreted antigensvaccine development
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1621 - 1632
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Ahmed, S. F., Oswald, I. P., Caspar, P., Hieny, S., Keefer, L., Sher, A. and James, S. L. (1997). Developmental differences determine larval susceptibility to nitric oxide-mediated killing in a murine model of vaccination against Schistosoma mansoni. Infection and Immunity 65, 219–226.CrossRefGoogle Scholar
Anderson, S., Coulson, P. S., Ljubojevic, S., Mountford, A. P. and Wilson, R. A. (1999). The radiation-attenuated schistosome vaccine induces high levels of protective immunity in the absence of B cells. Immunology 96, 22–28.CrossRefGoogle ScholarPubMed
Bazin, H., Beckers, A. and Querinjean, P. (1974). Three classes and four (sub)classes of rat immunoglobulins: IgM, IgA, IgE and IgG1, IgG2a, IgG2b, IgG2c. European Journal of Immunology 4, 44–48.CrossRefGoogle ScholarPubMed
Bergquist, N. R. and Colley, D. G. (1998). Schistosomiasis vaccine: research to development. Parasitology Today 14, 99–104.CrossRefGoogle ScholarPubMed
Bergquist, N. R., Leonardo, L. R. and Mitchell, G. F. (2005). Vaccine-linked chemotherapy: can schistosomiasis control benefit from an integrated approach? Trends in Parasitology 21, 112–117.CrossRefGoogle ScholarPubMed
Bethony, J. M., Diemert, D. J., Oliveira, S. C. and Loukas, A. (2008). Can schistosomiasis really be consigned to history without a vaccine? Vaccine 26, 3373–3376.CrossRefGoogle ScholarPubMed
Bickle, Q., Bain, J., McGregor, A. and Doenhoff, M. (1979 a). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse: III. The failure of primary infections with cercariae of one sex to induce resistance to reinfection. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 37–41.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J., Doenhoff, M. J., Ford, M. J. and Taylor, M. G. (1985). Resistance against Schistosoma mansoni induced by highly irradiated infections: studies on species specificity of immunization and attempts to transfer resistance. Parasitology 90, 301–312.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J. and Taylor, M. G. (1986). Schistosoma mansoni: characterization of two protective monoclonal antibodies. Parasite Immunology 8, 95–107.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Dobinson, T. and James, E. R. (1979 b). The effects of gamma-irradiation on migration and survival of Schistosoma mansoni schistosomula in mice. Parasitology 79, 223–230.CrossRefGoogle ScholarPubMed
Bickle, Q. D. and 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, 2101–2106.CrossRefGoogle ScholarPubMed
Bickle, Q. D. and Oldridge, J. (1999). Characterization of a stage-specific Mr16000 schistosomular surface glycoprotein antigen of Schistosoma mansoni. Molecular and Biochemical Parasitology 100, 85–94.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Taylor, M. G., Doenhoff, M. J. and Nelson, G. S. (1979 c). Immunization of mice with gamma-irradiated intramuscularly injected schistosomula of Schistosoma mansoni. Parasitology 79, 209–222.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Taylor, M. G., James, E. R., Nelson, G. S., Hussein, M. F., Andrews, B. J., Dobinson, A. R. and Marshall, T. F. (1979 d). Further observations on immunization of sheep against Schistosoma mansoni and S. bovis using irradiation-attenuated schistosomula of homologous and heterologous species. Parasitology 78, 185–193.CrossRefGoogle ScholarPubMed
Braschi, S., Borges, W. C. and Wilson, R. A. (2006). Proteomic analysis of the schistosome tegument and its surface membranes. Memórias do Instituto Oswaldo Cruz 101 (Suppl. 1), 205–212.CrossRefGoogle ScholarPubMed
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular and Cellular Proteomics 5, 347–356.CrossRefGoogle ScholarPubMed
Bushara, H. O., Hussein, M. F., Saad, A. M., Taylor, M. G., Dargie, J. D., Marshall, T. F. and Nelson, G. S. (1978). Immunization of calves against Schistosoma bovis using irradiated cercariae of schistosomula of S. bovis. Parasitology 77, 303–311.CrossRefGoogle ScholarPubMed
Cardoso, F. C., Macedo, G. C., Gava, E., Kitten, G. T., Mati, V. L., De Melo, A. L., Caliari, M. V., Almeida, G. T., Venancio, T. M., Verjovski-Almeida, S. and Oliveira, S. C. (2008). Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Neglected Tropical Diseases 2, e308.CrossRefGoogle ScholarPubMed
Caulada-Benedetti, Z., Al-Zamel, F., Sher, A. and James, S. (1991). Comparison of Th1- and Th2-associated immune reactivities stimulated by single versus multiple vaccination of mice with irradiated Schistosoma mansoni cercariae. Journal of Immunology 146, 1655–1660.CrossRefGoogle ScholarPubMed
Constant, S. L., Mountford, A. P. and Wilson, R. A. (1990). Phenotypic analysis of the cellular responses in regional lymphoid organs of mice vaccinated against Schistosoma mansoni. Parasitology 101, 15–22.CrossRefGoogle ScholarPubMed
Coulson, P. S. (1997). The radiation-attenuated vaccine against schistosomes in animal models: paradigm for a human vaccine? Advances in Parasitology 39, 271–336.CrossRefGoogle ScholarPubMed
Coulson, P. S. and Mountford, A. P. (1989). Fate of attenuated schistosomula administered to mice by different routes, relative to the immunity induced against Schistosoma mansoni. Parasitology 99, 39–45.CrossRefGoogle Scholar
Coulson, P. S., Smythies, L. E., Betts, C., Mabbott, N. A., Sternberg, J. M., Wei, X. G., Liew, F. Y. and Wilson, R. A. (1998). Nitric oxide produced in the lungs of mice immunized with the radiation-attenuated schistosome vaccine is not the major agent causing challenge parasite elimination. Immunology 93, 55–63.CrossRefGoogle Scholar
Coulson, P. S. and Wilson, R. A. (1988). Examination of the mechanisms of pulmonary phase resistance to Schistosoma mansoni in vaccinated mice. American Journal of Tropical Medicine and Hygiene 38, 529–539.CrossRefGoogle ScholarPubMed
Coulson, P. S. and Wilson, R. A. (1997). Recruitment of lymphocytes to the lung through vaccination enhances the immunity of mice exposed to irradiated schistosomes. Infection and Immunity 65, 42–48.CrossRefGoogle Scholar
Crabtree, J. E. and Wilson, R. A. (1986). The role of pulmonary cellular reactions in the resistance of vaccinated mice to Schistosoma mansoni. Parasite Immunology 8, 265–285.CrossRefGoogle ScholarPubMed
Dalton, J. P., Tom, T. D. and Strand, M. (1987). Cloning of a cDNA encoding a surface antigen of Schistosoma mansoni schistosomula recognized by sera of vaccinated mice. Proceedings of the National Academy of Sciences, USA 84, 4268–4272.CrossRefGoogle ScholarPubMed
Dean, D. A. (1983). Schistosoma and related genera: acquired resistance in mice. Experimental Parasitology 55, 1–104.CrossRefGoogle ScholarPubMed
Dean, D. A., Cioli, D. and Bukowski, M. A. (1981). Resistance induced by normal and irradiated Schistosoma mansoni: ability of various worm stages to serve as inducers and targets in mice. American Journal of Tropical Medicine and Hygiene 30, 1026–1032.CrossRefGoogle ScholarPubMed
Dean, D. A. and Mangold, B. L. (1992). Evidence that both normal and immune elimination of Schistosoma mansoni take place at the lung stage of migration prior to parasite death. American Journal of Tropical Medicine and Hygiene 47, 238–248.CrossRefGoogle Scholar
Dean, D. A., Mangold, B. L., Georgi, J. R. and 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. and McLaren, D. J. (1990). Evidence for enhancement of IgG1 subclass expression in mice polyvaccinated with radiation-attenuated cercariae of Schistosoma mansoni and the role of this isotype in serum-transferred immunity. Parasite Immunology 12, 15–32.CrossRefGoogle ScholarPubMed
Eberl, M., Langermans, J. A., Frost, P. A., Vervenne, R. A., Van Dam, G. J., Deelder, A. M., Thomas, A. W., Coulson, P. S. and Wilson, R. A. (2001). Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infection and Immunity 69, 5352–5362.CrossRefGoogle ScholarPubMed
Fenwick, A. and Webster, J. P. (2006). Schistosomiasis: challenges for control, treatment and drug resistance. Current Opinion in Infectious Diseases 19, 577–582.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D. and Taylor, M. G. (1984 a). Immunization of rats against Schistosoma mansoni using irradiated cercariae, lung schistosomula and liver-stage worms. Parasitology 89, 327–344.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D. and Taylor, M. G. (1987 a). Immunity to Schistosoma mansoni in congenitally athymic, irradiated and mast cell-depleted rats. Parasitology 94, 313–326.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D., Taylor, M. G. and Andrews, B. J. (1984 b). 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, 461–482.CrossRefGoogle ScholarPubMed
Ford, M. J., Dissous, C., Pierce, R. J., Taylor, M. G., Bickle, Q. D. and Capron, A. (1987 b). The isotypes of antibody responsible for the ‘late’ passive transfer of immunity in rats vaccinated with highly irradiated cercariae. Parasitology 94, 509–522.CrossRefGoogle ScholarPubMed
Francis, P. and Bickle, Q. (1992). Cloning of a 21·7-kDa vaccine-dominant antigen gene of Schistosoma mansoni reveals an EF hand-like motif. Molecular and Biochemical Parasitology 50, 215–224.CrossRefGoogle ScholarPubMed
Hagan, P., Ndhlovu, P. D. and Dunne, D. W. (1998). Schistosome immunology: more questions than answers. Parasitology Today 14, 407–412.CrossRefGoogle ScholarPubMed
Harrison, R. A., Bickle, Q. D., Kiare, S., James, E. R., Andrews, B. J., Sturrock, R. F., Taylor, M. G. and Webbe, G. (1990). Immunization of baboons with attenuated schistosomula of Schistosoma haematobium: levels of protection induced by immunization with larvae irradiated with 20 and 60 krad. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 89–99.CrossRefGoogle ScholarPubMed
Harrop, R., Coulson, P. S. and Wilson, R. A. (1999). Characterization, cloning and immunogenicity of antigens released by lung-stage larvae of Schistosoma mansoni. Parasitology 118, 583–594.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Hamblin, P. A. and Mountford, A. P. (2005). Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunology 27, 271–280.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Hamblin, P. A. and Mountford, A. P. (2007). In the absence of CD154, administration of interleukin-12 restores Th1 responses but not protective immunity to Schistosoma mansoni. Infection and Immunity 75, 3539–3547.CrossRefGoogle Scholar
Hoffmann, K. F., James, S. L., Cheever, A. W. and Wynn, T. A. (1999). Studies with double cytokine-deficient mice reveal that highly polarized Th1- and Th2-type cytokine and antibody responses contribute equally to vaccine-induced immunity to Schistosoma mansoni. Journal of Immunology 163, 927–938.CrossRefGoogle ScholarPubMed
Hsu, H. F., Hsu, S. Y. and Osborne, J. W. (1962). Immunization against Schistosoma japonicum in rhesus monkeys produced by irradiated cercariae. Nature, London 194, 98–99.CrossRefGoogle ScholarPubMed
Hsu, S. Y., Hsu, H. F. and Burmeister, L. F. (1981). Schistosoma mansoni: vaccination of mice with highly x-irradiated cercariae. Experimental Parasitology 52, 91–104.CrossRefGoogle ScholarPubMed
Hsu, S. Y., Hsu, H. F. and Osborn, J. W. (1969). Immunization of rhesus monkeys against schistosome infection by cercariae exposed to high doses of x-radiation. Proceedings of the Society of Experimental Biology and Medicine 131, 1146–1149.CrossRefGoogle ScholarPubMed
Hsu, S. Y., Xu, S. T., He, Y. X., Shi, F. H., Shen, W., Hsu, H. F., Osborne, J. W. and Clarke, W. R. (1984). Vaccination of bovines against schistosomiasis japonica with highly irradiated schistosomula in China. American Journal of Tropical Medicine and Hygiene 33, 891–898.CrossRefGoogle ScholarPubMed
James, S. L., Cheever, A. W., Caspar, P. and Wynn, T. A. (1998). Inducible nitric oxide synthase-deficient mice develop enhanced type 1 cytokine-associated cellular and humoral immune responses after vaccination with attenuated Schistosoma mansoni cercariae but display partially reduced resistance. Infection and Immunity 66, 3510–3518.CrossRefGoogle ScholarPubMed
James, S. L., Labine, M. and Sher, A. (1981). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. I. Analysis of antibody and T-lymphocyte responses in mouse strains developing differing levels of immunity. Cellular Immunology 65, 75–83.CrossRefGoogle ScholarPubMed
James, S. L., Pearce, E. J. and Sher, A. (1985). Induction of protective immunity against Schistosoma mansoni by a non living vaccine. I. Partial characterization of antigens recognized by antibodies from mice immunized with soluble schistosome extracts. Journal of Immunology 134, 3432–3438.CrossRefGoogle ScholarPubMed
James, S. L. and 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, 567–575.CrossRefGoogle Scholar
Jankovic, D., Wynn, T. A., Kullberg, M. C., Hieny, S., Caspar, P., James, S., Cheever, A. W. and Sher, A. (1999). Optimal vaccination against Schistosoma mansoni requires the induction of both B cell- and IFN-gamma-dependent effector mechanisms. Journal of Immunology 162, 345–351.CrossRefGoogle Scholar
Jarrett, W. F., Jennings, F. W., McIntyre, W., Mulligan, W. and Urquhart, G. M. (1958). Irradiated helminth larvae in vaccination. Proceedings of the Royal Society of Medicine 51, 743–744.CrossRefGoogle ScholarPubMed
Jwo, J. and LoVerde, P. T. (1989). The ability of fractionated sera from animals vaccinated with irradiated cercariae of Schistosoma mansoni to transfer immunity to mice. Journal of Parasitology 75, 252–260.CrossRefGoogle ScholarPubMed
Kallenius, G., Pawlowski, A., Brandtzaeg, P. and Svenson, S. (2007). Should a new tuberculosis vaccine be administered intranasally? Tuberculosis 87, 257–266.CrossRefGoogle ScholarPubMed
Kamiya, H., Smithers, S. R. and McLaren, D. J. (1987). Schistosoma mansoni: autoradiographic tracking studies of isotopically-labelled challenge parasites in naive and vaccinated CBA/Ca mice. Parasite Immunology 9, 515–529.CrossRefGoogle ScholarPubMed
Kariuki, T. M., Farah, I. O., Yole, D. S., Mwenda, J. M., Van Dam, G. J., Deelder, A. M., Wilson, R. A. and Coulson, P. S. (2004). Parameters of the attenuated schistosome vaccine evaluated in the olive baboon. Infection and Immunity 72, 5526–5529.CrossRefGoogle ScholarPubMed
Kariuki, T. M., Van Dam, G. J., Deelder, A. M., Farah, I. O., Yole, D. S., Wilson, R. A. and Coulson, P. S. (2006). Previous or ongoing schistosome infections do not compromise the efficacy of the attenuated cercaria vaccine. Infection and Immunity 74, 3979–3986.CrossRefGoogle Scholar
Kassim, O. O., Dean, D. A., Mangold, B. L. and Von Lichtenberg, F. (1992). Combined microautoradiographic and histopathologic analysis of the fate of challenge Schistosoma mansoni schistosomula in mice immunized with irradiated cercariae. American Journal of Tropical Medicine and Hygiene 47, 231–237.CrossRefGoogle ScholarPubMed
Kelly, E. A. and Colley, D. G. (1988). In vivo effects of monoclonal anti-L3T4 antibody on immune responsiveness of mice infected with Schistosoma mansoni. Reduction of irradiated cercariae-induced resistance. Journal of Immunology 140, 2737–2745.CrossRefGoogle ScholarPubMed
Lawson, B. W., Bickle, Q. D. and Taylor, M. G. (1993). Mechanisms involved in the loss of antibody-mediated adherence of macrophages to lung-stage schistosomula of Schistosoma mansoni in vitro. Parasitology 106, 463–469.CrossRefGoogle ScholarPubMed
Lewis, F. A. and Wilson, E. M. (1982). Regional and splenic lymphocyte proliferative responses of mice exposed to normal or irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 31, 505–513.CrossRefGoogle ScholarPubMed
Loukas, A., Tran, M. and Pearson, M. S. (2007). Schistosome membrane proteins as vaccines. International Journal of Parasitology 37, 257–263.CrossRefGoogle ScholarPubMed
Majid, A. A., Bushara, H. O., Saad, A. M., Hussein, M. F., Taylor, M. G., Dargie, J. D., Marshall, T. F. and Nelson, G. S. (1980). Observations on cattle schistosomiasis in the Sudan, a study in comparative medicine. III. Field testing of an irradiated Schistosoma bovis vaccine. American Journal of Tropical Medicine and Hygiene 29, 452–455.CrossRefGoogle Scholar
Mangold, B. L. and 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, 249–265.CrossRefGoogle Scholar
Mangold, B. L. and Dean, D. A. (1986). Passive transfer with serum and IgG antibodies of irradiated cercaria-induced resistance against Schistosoma mansoni in mice. Journal of Immunology 136, 2644–2648.CrossRefGoogle ScholarPubMed
Mangold, B. L. and Dean, D. A. (1992). The role of IgG antibodies from irradiated cercaria-immunized rabbits in the passive transfer of immunity to Schistosoma mansoni-infected mice. American Journal of Tropical Medicine and Hygiene 47, 821–829.CrossRefGoogle ScholarPubMed
Mangold, B. L., Dean, D. A., Coulson, P. S. and 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, 332–344.CrossRefGoogle ScholarPubMed
Mangold, B. L. and Knopf, P. M. (1981). Host protective humoral immune responses to Schistosoma mansoni infections in the rat. Kinetics of hyperimmune serum-dependent sensitivity and elimination of schistosomes in a passive transfer system. Parasitology 83, 559–574.CrossRefGoogle Scholar
Mastin, A., Bickle, Q. D. and Wilson, R. A. (1985). An ultrastructural examination of irradiated, immunizing schistosomula of Schistosoma mansoni during their extended stay in the lungs. Parasitology 91, 101–110.CrossRefGoogle ScholarPubMed
Mastin, A. J., Bickle, Q. D. and 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., Pearce, E. J. and 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. and 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. and 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, 287–302.Google ScholarPubMed
McManus, D. P. and Loukas, A. (2008). Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225–242.CrossRefGoogle ScholarPubMed
Miller, T. A. (1978). Industrial development and field use of the canine hookworm vaccine. Advances in Parasitology 16, 333–342.CrossRefGoogle ScholarPubMed
Minard, P., Dean, D. A., Jacobson, R. H., Vannier, W. E. and Murrell, K. D. (1978 a). Immunization of mice with cobalt-60 irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 76–86.CrossRefGoogle ScholarPubMed
Minard, P., Dean, D. A., Vannier, W. E. and Murrell, K. D. (1978 b). Effect of immunization on migration of Schistosoma mansoni through lungs. American Journal of Tropical Medicine and Hygiene 27, 87–93.CrossRefGoogle ScholarPubMed
Moloney, N. A. and Webbe, G. (1990). Antibody is responsible for the passive transfer of immunity to mice from rabbits, rats or mice vaccinated with attenuated Schistosoma japonicum cercariae. Parasitology 100, 235–239.CrossRefGoogle ScholarPubMed
Moser, G., Wassom, D. L. and 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 parasite antigens by host molecules. Journal of Experimental Medicine 152, 41–53.CrossRefGoogle Scholar
Mountford, A. P., Anderson, S. and Wilson, R. A. (1996). Induction of Th1 cell-mediated protective immunity to Schistosoma mansoni by co-administration of larval antigens and IL-12 as an adjuvant. Journal of Immunology 156, 4739–4745.CrossRefGoogle ScholarPubMed
Mountford, A. P., Coulson, P. S., Pemberton, R. M., Smythies, L. E. and Wilson, R. A. (1992). The generation of interferon-gamma-producing T lymphocytes in skin-draining lymph nodes, and their recruitment to the lungs, is associated with protective immunity to Schistosoma mansoni. Immunology 75, 250–256.Google Scholar
Mountford, A. P., Coulson, P. S. and Wilson, R. A. (1988). Antigen localization and the induction of resistance in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology 97, 11–25.CrossRefGoogle ScholarPubMed
Oswald, I. P., Caspar, P., Wynn, T. A., Scharton-Kersten, T., Williams, M. E., Hieny, S., Sher, A. and James, S. L. (1998). Failure of P strain mice to respond to vaccination against schistosomiasis correlates with impaired production of IL-12 and up-regulation of Th2 cytokines that inhibit macrophage activation. European Journal of Immunology 28, 1762–1772.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Pearce, E. J., Basch, P. F. and 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, 79–94.CrossRefGoogle ScholarPubMed
Pearce, E. J., Caspar, P., Grzych, J. M., Lewis, F. A. and Sher, A. (1991). Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. Journal of Experimental Medicine 173, 159–166.CrossRefGoogle ScholarPubMed
Pemberton, R. M., Smythies, L. E., Mountford, A. P. and Wilson, R. A. (1991). Patterns of cytokine production and proliferation by T lymphocytes differ in mice vaccinated or infected with Schistosoma mansoni. Immunology 73, 327–333.Google ScholarPubMed
Pemberton, R. M. and Wilson, R. A. (1995). T-helper type-1-dominated lymph node responses induced in C57BL/6 mice by optimally irradiated cercariae of Schistosoma mansoni are down-regulated after challenge infection. Immunology 84, 310–316.Google ScholarPubMed
Radke, M. G. and Sadun, E. H. (1963). Resistance produced in mice by exposure to irradiated Schistosoma mansoni cercariae. Experimental Parasitology 13, 134–142.CrossRefGoogle Scholar
Reynolds, S. R. and Harn, D. A. (1992). Comparison of irradiated-cercaria schistosome vaccine models that use 15- and 50-kilorad doses: the 15-kilorad dose gives greater protection, smaller liver sizes, and higher gamma interferon levels after challenge. Infection and Immunity 60, 90–94.CrossRefGoogle ScholarPubMed
Richter, D. and Harn, D. A. (1993). Candidate vaccine antigens identified by antibodies from mice vaccinated with 15- or 50-kilorad-irradiated cercariae of Schistosoma mansoni. Infection and Immunity 61, 146–154.CrossRefGoogle ScholarPubMed
Richter, D., Incani, R. N. and Harn, D. A. (1993 a). Isotype responses to candidate vaccine antigens in protective sera obtained from mice vaccinated with irradiated cercariae of Schistosoma mansoni. Infection and Immunity 61, 3003–3011.CrossRefGoogle ScholarPubMed
Richter, D., Reynolds, S. R. and Harn, D. A. (1993 b). Candidate vaccine antigens that stimulate the cellular immune response of mice vaccinated with irradiated cercariae of Schistosoma mansoni. Journal of Immunology 151, 256–265.CrossRefGoogle ScholarPubMed
Sadun, E. H., Bruce, J. I. and Macomber, P. B. (1964). Parasitologic, pathologic and serologic reactions to Schistosoma mansoni in monkeys exposed to irradiated cercariae. American Journal of Tropical Medicine and Hygiene 13, 548–557.CrossRefGoogle ScholarPubMed
Sher, A., Hieny, S., James, S. L. and Asofsky, R. (1982 a). 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, 1880–1884.CrossRefGoogle ScholarPubMed
Sher, A., James, S. L., Simpson, A. J., Lazdins, J. K. and Meltzer, M. S. (1982 b). Macrophages as effector cells of protective immunity in murine schistosomiasis. III. Loss of susceptibility to macrophage-mediated killing during maturation of S. mansoni schistosomula from the skin to the lung stage. Journal of Immunology 128, 1876–1879.CrossRefGoogle Scholar
Simpson, A. J., James, S. L. and Sher, A. (1983). Identification of surface antigens of schistosomula of Schistosoma mansoni recognized by antibodies from mice immunized by chronic infection and by exposure to highly irradiated cercariae. Infection and Immunity 41, 591–597.CrossRefGoogle ScholarPubMed
Smithers, S. R. (1962). Immunizing effect of irradiated cercariae of Schistosoma mansoni in rhesus monkeys. Nature, London 194, 1146–1147.CrossRefGoogle ScholarPubMed
Smithers, S. R. (1976). Immunity to trematode infections. In Immunology of Parasitic Infections (ed. Cohen, E. and Sadun, E. E.), pp. 296–332. Blackwell Scientific Publications, Oxford, UK.Google Scholar
Smithers, S. R. and Terry, R. J. (1965). Naturally acquired resistance to experimental infections of Schistosoma mansoni in the rhesus monkey (Macaca mulatta). Parasitology 55, 701–710.CrossRefGoogle ScholarPubMed
Smithers, S. R. and Terry, R. J. (1967). Resistance to experimental infection with Schistosoma mansoni in rhesus monkeys induced by the transfer of adult worms. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 517–533.CrossRefGoogle ScholarPubMed
Smyth, D., McManus, D. P., Smout, M. J., Laha, T., Zhang, W. and Loukas, A. (2003). Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infection and Immunity 71, 2548–2554.CrossRefGoogle ScholarPubMed
Smythies, L. E., Betts, C., Coulson, P. S., Dowling, M. A. and Wilson, R. A. (1996). Kinetics and mechanism of effector focus formation in the lungs of mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasite Immunology 18, 359–369.CrossRefGoogle ScholarPubMed
Smythies, L. E., Coulson, P. S. and Wilson, R. A. (1992 a). Monoclonal antibody to IFN-gamma modifies pulmonary inflammatory responses and abrogates immunity to Schistosoma mansoni in mice vaccinated with attenuated cercariae. Journal of Immunology 149, 3654–3658.CrossRefGoogle ScholarPubMed
Smythies, L. E., Pemberton, R. M., Coulson, P. S., Mountford, A. P. and Wilson, R. A. (1992 b). T cell-derived cytokines associated with pulmonary immune mechanisms in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Journal of Immunology 148, 1512–1518.CrossRefGoogle ScholarPubMed
Soisson, L. A., Reid, G. D., Farah, I. O., Nyindo, M. and Strand, M. (1993). Protective immunity in baboons vaccinated with a recombinant antigen or radiation-attenuated cercariae of Schistosoma mansoni is antibody-dependent. Journal of Immunology 151, 4782–4789.CrossRefGoogle ScholarPubMed
Soisson, L. M., Masterson, C. P., Tom, T. D., McNally, M. T., Lowell, G. H. and Strand, M. (1992). Induction of protective immunity in mice using a 62-kDa recombinant fragment of a Schistosoma mansoni surface antigen. Journal of Immunology 149, 3612–3620.CrossRefGoogle ScholarPubMed
Stek, M. Jr., Dean, D. A. and Clark, S. S. (1981 a). Attrition of schistosomes in an irradiation-attenuated cercarial immunization model of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 30, 1033–1038.CrossRefGoogle Scholar
Stek, M. F., Minard, P., Dean, D. A. and Hall, J. E. (1981 b). Immunization of baboons with Schistosoma mansoni cercariae attenuated by gamma irradiation. Science 212, 1518–1520.CrossRefGoogle Scholar
Sturrock, R. F., James, C., James, E. R. and Webbe, G. (1980). Immunization of baboons (Papio anubis) against Schistosoma haematobium with irradiated cercariae or schistosomula. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 834–835.CrossRefGoogle ScholarPubMed
Taylor, M. G. (1994). Schistosomiasis vaccines: Farewell to the God of Plague? Journal of Tropical Medicine and Hygiene 97, 257–268.Google ScholarPubMed
Taylor, M. G., James, E. R., Nelson, G. S., Bickle, Q., Andrews, B. J., Dobinson, A. R. and Webbe, G. (1976 a). Immunisation of baboons against Schistosoma mansoni using irradiated S. mansoni cercariae and schistosomula and non-irradiated S. rodhaini cercariae. Journal of Helminthology 50, 215–221.CrossRefGoogle ScholarPubMed
Taylor, M. G., James, E. R., Nelson, G. S., Bickle, Q., Dunne, D. W. and Webbe, G. (1976 b). Immunisation of sheep against Schistosoma mattheei using either irradiated cercariae or irradiated schistosomula. Journal of Helminthology 50, 1–9.CrossRefGoogle ScholarPubMed
Tran, M. H., Pearson, M. S., Bethony, J. M., Smyth, D. J., Jones, M. K., Duke, M., Don, T. A., McManus, D. P., Correa-Oliveira, R. and Loukas, A. (2006). Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Medicine 12, 835–840.CrossRefGoogle ScholarPubMed
Vignali, D. A., Bickle, Q. D. and Taylor, M. G. (1988 a). 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., Bickle, Q. D., Taylor, M. G., Tennent, G. and Pepys, M. B. (1988 b). Comparison of the role of complement in immunity to Schistosoma mansoni in rats and mice. Immunology 63, 55–61.Google ScholarPubMed
Vignali, D. A., Crocker, P., Bickle, Q. D., Cobbold, S., Waldmann, H. and Taylor, M. G. (1989 a). A role for CD4+ but not CD8+ T cells in immunity to Schistosoma mansoni induced by 20 krad-irradiated and Ro 11-3128-terminated infections. Immunology 67, 466–472.Google Scholar
Vignali, D. A., Klaus, S. N., Bickle, Q. D. and Taylor, M. G. (1989 b). 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
Villella, J. B., Gomberg, H. J. and Gould, S. E. (1961). Immunization to Schistosoma mansoni in mice inoculated with radiated cercariae. Science 134, 1073–1075.CrossRefGoogle ScholarPubMed
Von Lichtenberg, F., Correa-Oliveira, R. and Sher, A. (1985). The fate of challenge schistosomula in the murine anti-schistosome vaccine model. American Journal of Tropical Medicine and Hygiene 34, 96–106.CrossRefGoogle ScholarPubMed
Webbe, G., Sturrock, R. F., James, E. R. and James, C. (1982). Schistosoma haematobium in the baboon (Papio anubis): effect of vaccination with irradiated larvae on the subsequent infection with percutaneously applied cercariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 354–361.CrossRefGoogle ScholarPubMed
Wilson, R. A. and Coulson, P. S. (1989). Lung-phase immunity to Schistosomes: a new perspective on an old problem? Parasitology Today 5, 274–278.CrossRefGoogle Scholar
Wilson, R. A. and Coulson, P. S. (2006). Schistosome vaccines: a critical appraisal. Memórias do Instituto Oswaldo Cruz 101 (Suppl. 1), 13–20.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S., Betts, C., Dowling, M. A. and Smythies, L. E. (1996). Impaired immunity and altered pulmonary responses in mice with a disrupted interferon-gamma receptor gene exposed to the irradiated Schistosoma mansoni vaccine. Immunology 87, 275–282.CrossRefGoogle Scholar
Wilson, R. A., Coulson, P. S. and 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, 101–116.CrossRefGoogle ScholarPubMed
Wynn, T. A., Jankovic, D., Hieny, S., Cheever, A. W. and Sher, A. (1995). IL-12 enhances vaccine-induced immunity to Schistosoma mansoni in mice and decreases T helper 2 cytokine expression, IgE production, and tissue eosinophilia. Journal of Immunology 154, 4701–4709.CrossRefGoogle ScholarPubMed
Wynn, T. A., Oswald, I. P., Eltoum, I. A., Caspar, P., Lowenstein, C. J., Lewis, F. A., James, S. L. and Sher, A. (1994). Elevated expression of Th1 cytokines and nitric oxide synthase in the lungs of vaccinated mice after challenge infection with Schistosoma mansoni. Journal of Immunology 153, 5200–5209.CrossRefGoogle ScholarPubMed
Wynn, T. A., Reynolds, A., James, S., Cheever, A. W., Caspar, P., Hieny, S., Jankovic, D., Strand, M. and Sher, A. (1996). IL-12 enhances vaccine-induced immunity to schistosomes by augmenting both humoral and cell-mediated immune responses against the parasite. Journal of Immunology 157, 4068–4078.CrossRefGoogle ScholarPubMed
Yole, D. S., Reid, G. D. and Wilson, R. A. (1996). Protection against Schistosoma mansoni and associated immune responses induced in the vervet monkey Cercopithecus aethiops by the irradiated cercaria vaccine. American Journal of Tropical Medicine and Hygiene 54, 265–270.CrossRefGoogle ScholarPubMed