Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T02:56:59.416Z Has data issue: false hasContentIssue false

Phenotypic analysis of the cellular responses in regional lymphoid organs of mice vaccinated against Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

S. L. Constant
Affiliation:
Department of Biology, University of York, York YO1 5DD, UK
A. P. Mountford
Affiliation:
Department of Biology, University of York, York YO1 5DD, UK
R. A. Wilson
Affiliation:
Department of Biology, University of York, York YO1 5DD, UK

Summary

The cellular responses in regional lymphoid organs of C57B1/6 mice were examined, following protective immunization with 20 krad.-irradiated cercariae of S. mansoni. Marked changes in total cell number were observed, with peak increases of 13·5-fold in the skin-draining (axillary) lymph nodes and 6·9-fold in the lung-draining (mediastinal) lymph nodes. In contrast, cellular responses were small in the spleen and undetectable in the brachial lymph nodes. The temporal pattern of responses was coincident with the kinetics of parasite migration, events in the mediastinal lymph node being apparent only after day 7. Phenotypic analysis of the cellular changes revealed an increase both in T lymphocytes and, to a greater extent, in B lymphocytes. The changes in Thyl+ cells comprised an increase in both L3T4+ and Lyt2+ populations. A comparison of mice exposed to non-immunizing parasites (normal or 80 krad.-irradiated cercariae) with protected animals, revealed smaller and more transient cellular changes in the axillary lymph nodes of the former. We suggest that the successful immunization of mice with attenuated parasites depends upon the prolonged priming of lymphocytes within the lymph nodes draining the skin-exposure site and that the persistence of 20 krad.-irradiated parasites within these nodes provides the requisite stimulus.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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

Aitken, R., Coulson, P. S. & Wilson, R. A. (1988). Pulmonary leukocytic responses are linked to the acquired immunity of mice vaccinated with irradiated cercariae of Schistosoma mansoni. Journal of Immunology 140, 3573–9.CrossRefGoogle Scholar
Austyn, J. M. (1989). Antigen-Presenting Cells (ed. Male, D.). Oxford: IRL Press.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.CrossRefGoogle ScholarPubMed
Bottomly, K. & Janeway, C. A. Jr (1989). Antigen presentation by B cells. Nature, London 337, 24.CrossRefGoogle ScholarPubMed
Cher, D. J. & Mosmann, T. R. (1987). Two types of murine helper T cell clone. II. Delayed-type hypersensitivity is mediated by Th1 clones. Journal of Immunology 138, 3688–94.CrossRefGoogle ScholarPubMed
Correa-oliveira, R., Sher, A. & James, S. L. (1984). Defective vaccine-induced immunity to Schistosoma mansoni in P strain mice. I. Analysis of antibody responses. Journal of Immunology 133, 1581–6.CrossRefGoogle Scholar
Coulson, P. S. & Mountford, A. P. (1989). Fate of attenuated schistosomula administered to mice by different routes, relative to the immunity induced against Schistosoma mansoni. Parasitology 99, 3945.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Drayson, M. T., Smith, M. E. & Ford, W. L. (1981). The sequence of changes in blood flow and lymphocyte influx to stimulated rat lymph nodes. Immunology 44, 125–33.Google ScholarPubMed
Heinzel, F. P., Sadik, M. D., Holaday, B. J., Coffman, R. L. & Locksley, R. M. (1989). Reciprocal expression of interferon or interleukin 4 during the resolution or progression of murine leishmaniasis. Journal of Experimental Medicine 169, 5972.CrossRefGoogle ScholarPubMed
Hunt, S. V. (1987). Preparation of lymphocytes and accessory cells. In Lymphocytes: a Practical Approach (ed. Klaus, G. G. B.) pp. 134. Oxford: IRL Press.Google 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., Glaven, 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 137, 3959–67.CrossRefGoogle 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 antibody and T-lymphocyte responses in mouse strains developing differing levels of immunity. Cellular Immunology 65, 7583.CrossRefGoogle ScholarPubMed
Janeway, C. A. Jr, Ron, J. & Katz, M. E. (1987). The B cell is the initiating antigen-presenting cell in peripheral lymph nodes. Journal of Immunology 138, 1051–5.CrossRefGoogle Scholar
Lanzavecchia, A. (1985). Antigen-specific interaction between T and B cells. Nature, London 314, 537–9.CrossRefGoogle ScholarPubMed
Lewis, F. A. & 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, 505–13.CrossRefGoogle ScholarPubMed
Lynch, F., Doherty, P. C. & Ceredig, R. (1989). Phenotypic and functional analysis of the cellular response in regional lymphoid tissue during an acute virus infection. Journal of Immunology 142, 3592–8.CrossRefGoogle ScholarPubMed
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
Mason, L., Giardina, S. L., Hecht, T., Ortaldo, J. & Mathieson, B. J. (1988). LGL-1: a non-polymorphic antigen expressed on a major population of mouse natural killer cells. Journal of Immunology 140, 4403–12.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 91, 101–10.CrossRefGoogle ScholarPubMed
Menson, E. N., Coulson, P. S. & Wilson, R. A. (1989). Schistosoma mansoni: circulating and pulmonary leucocyte responses related to the induction of protective immunity in mice by irradiated parasites. Parasitology 98, 4355.CrossRefGoogle Scholar
Mosmann, T. R. & Coffman, R. L. (1987). Two types of mouse helper T-cell clone: implications for immune regulation. Immunology Today 8, 223–7.CrossRefGoogle ScholarPubMed
Mountford, A. P., Coulson, P. S. & Wilson, R. A. (1988). Antigen localization and the induction of resistance in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasitology 97, 1125.CrossRefGoogle ScholarPubMed
Olivier, L. & Stirewalt, M. A. (1952). An effective method for the exposure of mice to cercariae of Schistosoma mansoni. Journal of Parasitology 38, 1923.CrossRefGoogle Scholar
Pabst, R. (1988). The spleen in lymphocyte migration. Immunology Today 9, 43–5.CrossRefGoogle ScholarPubMed
Roberts, S. M., Boot, c. & Wilson, R. A. (1988). Antibody responses of rodents to a tegument membrane preparation from adult Schistosoma mansoni. Parasitology 97, 425–35.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
Wilson, R. A. (1987). Cercariae to liver worms: development and migration in the mammalian host. In The Biology of Schistosomes (ed. Rollinson, D. & Simpson, A. J. G.) pp. 115–46. London: Academic Press.Google Scholar
Wilson, R. A. & Coulson, P. S. (1986). Schistosoma mansoni: dynamics of migration through the vascular system of the mouse. Parasitology 92, 83100.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S. & Mchugh, S. M. (1983). A significant part of the ‘concomitant immunity’ of mice to Schistosoma mansoni is a consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595601.CrossRefGoogle Scholar
Yeh, C.-J. G., Hsi, B.-L. & Faulk, W. P. (1981). Propidium iodide as a nuclear marker in immunofluorescence. II. Use with cellular identification and viability studies. Journal of Immunological Methods 43, 269–75.CrossRefGoogle ScholarPubMed