Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-18T00:23:00.977Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosoma mansoni: evidence that eosinophils and/or macrophages contribute to skin-phase challenge attrition in vaccinated CBA/Ca mice

Published online by Cambridge University Press:  06 April 2009

Rosalind E. M. Ward  and
Diane J. McLaren
Rosalind E. M. Ward
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
Diane J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
Get access Rights & Permissions [Opens in a new window]

Summary

Naive CBA mice and mice vaccinated 4 weeks previously with gamma-irradiated cercariae were challenged percutaneoualy with normal cercariae and the skin site of challenge removed at various times to provide samples for histological examination. Neutrophil abscesses surrounding schistosomula as well as cast cercarial tails were identified at the skin surface in both naive/challenged and vaccinated/challenged mice. The dermis in both groups of animals became infiltrated with mononuclear cells and granulocytes. Neutrophils were the predominant granulocyte in naive/challenged skin but eosinophils replaced neutrophils by 48 h post-challenge in skin from vaccinated mice. Schistosomula with adherent mononuclear cells and granulocytes were identified preferentially in the dermis of vaccinated mice; such larvae frequently exhibited subtegumental vacuolation. A further major characteristic of vaccinated/challenged skin was the formation, from 18 h, of extensive subdermal inflammatory foci, consisting of up to 50% mononuclear cells and 50% eosinophils. These foci invariably surrounded one or more larval parasites which were seen by both optical and scanning electron microscopy to have a morphology typical of lung stage rather than skin stage schistosomula. Dead, infiltrated parasites were also recognized within the subdermal foci. Our data support the view that vaccine immunity in this mouse model is mediated primarily in the skin and indicate that challenge attrition involves immobilization and killing of larval parasites by effector cells within subdermal inflammatory foci.

Type
Research Article
Information
Parasitology , Volume 96 , Issue 1 , February 1988 , pp. 63 - 84
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

Auriault, C., Damonneville, M., Verwaerde, C., Pierce, R., Joseph, M., Capron, M. & Capron, A. (1984). Rat IgE directed against schistosomula-released products is cytotoxic for Schistosoma mansoni schistosomula in vitro. European Journal of Immunology 14, 132–8.CrossRefGoogle ScholarPubMed
Bentley, A. G., Carlisle, A. S. & Phillips, S. M. (1981). Ultrastructural analysis of the cellular response to Schistosoma mansoni. II. Inflammatory responses in rodent skin. American Journal of Tropical Medicine and Hygiene 30, 815–24.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Dobinson, T. & James, E. R. (1979). The effects of gamma-irradiation on migration and survival of Schistosoma mansoni schistosomula in mice. Parasitology 79, 223–30.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Wassom, D. L., Gleich, G. J., Loegering, D. A. & David, J. R. (1979). Damage to schistosomula of Schistosoma mansoni induced directly by major basic protein. Journal of Immunology 122, 221–9.CrossRefGoogle ScholarPubMed
Crabtree, J. E. & Wilson, R. A. (1980). Schistosoma mansoni: a scanning electron microscope study of the developing schistosomulum. Parasitology 81, 553–64.CrossRefGoogle ScholarPubMed
Damonneville, M., Auriault, C., Thorel, T., Verwaerde, C., Pierce, A., Strecker, G. & Capron, A. (1986). Induction of a protective immune IgE response in rats by injection of defined antigens of schistosomulum-released products: immunochemical properties of the target antigens. International Archives of Allergy and Applied Immunology 79, 320–8.CrossRefGoogle ScholarPubMed
Damonneville, M., Auriault, C., Verwaerde, C., Delanoye, A., Pierce, R. & Capron, A. (1986). Protection against experimental Schistosoma mansoni schistosomiasis achieved by immunization with schistosomula released products antigens (SRP-A): role of IgE antibodies. Clinical and Experimental Immunology 65, 244–52.Google 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
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, 13–25.CrossRefGoogle ScholarPubMed
Hsu, S. Y. L., Hsu, H. F., Johnson, S. C., Xu, S. T. & Johnson, S. M. (1983). Histopathological study of the attrition of challenge cercariae of Schistosoma mansoni in the skin of mice immunised by chronic infection and by use of highly X-irradiated cercariae. Zeitschrift für Parasitenkunde 69. 627–42.CrossRefGoogle ScholarPubMed
Incani, R. N. & McLaren, D J. (1984). Histopathological and ultrastructural studies of cutaneous reactions elicited in naive and chronically infected mice by invading schistosomula of Schistosoma mansoni. International Journal for Parasitology 14, 250–76.CrossRefGoogle ScholarPubMed
James, S. L. & Cheever, A. W. (1986). 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 Scholar
James, S. L., Correa-Oliveira, R. & Leonard, E. J. (1984). Defective vaccine-induced 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 vaccineinduced 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., Lazdins, J. K. & Meltzer, M. S. (1982). Macrophages as effector cells of protective immunity in murine schistosomiasis. II. Killing of newly transformed schistosomula by macrophages activated as a consequence of Schistosoma mansoni infection. Journal of Immunology 128, 1535–40.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
Karnovsky, M J. (1965). A formaldehyde-glutaraldehyde fixative of high molality for use in electron microscopy. Journal of Cell Biology 27, 137A.Google Scholar
Lanar, D. E., Pearce, E. J., James, S. L. & Sher, A. (1986). Identification of paramyosin as schistosome antigen recognised by intradermally vaccinated mice. Science 234, 593–6.CrossRefGoogle ScholarPubMed
Lichtenberg, F. von, Sher, A., Gibbons, N. & Doughty, B. (1976). Eosinophil-enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 84, 479–99.Google ScholarPubMed
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.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, 332–440.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. (1980 a). Schistosoma mansoni: the parasite surface in relation to host immunity. In Tropical Medicine Research Studies, vol. 1, (ed Brown, K. N.). Chichester: John Wiley/Research Studies Press.Google Scholar
McLaren, D. J. (1980 b). Ultrastructural observations on the interaction between host cells and Parasitic helminths. In The Host-Invader Interplay, vol. 2, (ed. Van den Bossche, H.), pp. 85–104. Amsterdam: Elsevier.Google Scholar
McLaren, D. J. (1980 c). Ultrastructural studies of eosinophils and their interaction with parasites. Transactions of the Royal Society for Tropical Medicine and Hygiene (Supp.) 74, 28–37.CrossRefGoogle Scholar
McLaren, D. J. (1984). Disguise as an evasive stratagem of parasitic organisms. Parasitology 88, 597–611.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature London 269, 147–9.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Incani, R. N. (1982). Schistosoma mansoni: acquired resistance by developing schistosomula to immune attack in vitro. Experimental Parasitology 53, 285–98.CrossRefGoogle ScholarPubMed
McLaren, D. J. & James, S. L. (1985). Ultrastructural studies of the killing of schistosomula of Schislosoma mansoni by activated macrophages in vitro. Parasite Immunology 7, 315–31.CrossRefGoogle ScholarPubMed
McLaren, D. J., McKean, J. R., Olsson, I., Venge, P. & Kay, A. B. (1981). Morphological studies on the killing of schistosomula of Schistosoma mansoni by human eosinophil and neutrophil cationic proteins in vitro. Parasite Immunology 3, 359–73.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., Peterson, C. G. B. & Venge, P. (1984). Schistosoma mansoni: further studies of the interaction between schistosomula and granulocyte-derived cationic proteins in vitro. Parasitology 88, 491–503.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.). London: Academic Press (in the 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 depletes cutaneous effector cells. Parasite Immunology (in the Press).CrossRefGoogle Scholar
McLaren, D. J. & Terry, R. J. (1982). The protective role of acquired host antigens during schistosome maturation. Parasite Immunology 4, 129–48.CrossRefGoogle ScholarPubMed
McLaren, D. J., Worms, M. J., Brown, S. J. & Askenase, P. W. (1983). Ornithodorus tartakovskyi: quantitation and ultrastructure of cutaneous basophil responses in the guinea pig. Experimental Parasitology 56, 153–68.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
Minard, P., Dean, D. A., Jacobson, R. H., Vannier, W. E. & Murrell, K. D. (1978). Immunization of mice with Cobalt-60 irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 76–93.CrossRefGoogle ScholarPubMed
Pearce, E. J. & McLaren, D. J. (1986). Schistosoma mansoni: the cutaneous response to cercarial challenge in naive guinea pigs and guinea pigs vaccinated with highly irradiated cercariae. International Journal for Parasitology 16, 491–510.CrossRefGoogle ScholarPubMed
Ramalho-Pinto, F. J., McLaren, D. J. & Smithers, S. R. (1978). Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils. Journal of Experimental Medicine 147, 147–56.CrossRefGoogle ScholarPubMed
Rumjanek, F. D. & McLaren, D. J. (1981). Schistosoma mansoni: modulation of schistosomular lipid composition by serum. Molecular and Biochemical Parasitology 3, 239–52.CrossRefGoogle ScholarPubMed
Rumjanek, F. D., McLaren, D. J. & Smithers, S. R. (1983). Serum-induced expression of a surface protein in schistosomula of Schistosoma mansoni: a possible receptor for lipid uptake. Molecular and Biochemical Parasitology 9, 337–50.CrossRefGoogle ScholarPubMed
Savage, A. M. & Colley, D. G. (1980). The eosinophil in the inflammatory response to cercarial challenge of sensitized and chronically infected CBA/J mice. American Journal of Tropical Medicine and Hygiene 29, 1268–78.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Doenhoff, M. J. (1982). Schistosomiasis. In Immunology of Parasitic Infections (ed. Cohen, S. and Warren, K. S.), pp. 527–607. Oxford: Blackwell Scientific PublicationsGoogle Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695–700.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