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. 1987 Jun;55(6):1339–1345. doi: 10.1128/iai.55.6.1339-1345.1987

Macrophage activation as an immune correlate to protective immunity against schistosomiasis in mice immunized with an irradiated, cryopreserved live vaccine.

F A Lewis, J Winestock, S L James
PMCID: PMC260517  PMID: 3106218

Abstract

Immune responses against Schistosoma mansoni were evaluated in C57BL/6 mice injected with one of two populations of irradiated schistosomules, the larval preparations differing only in the degree of freezing-induced damage sustained upon cryopreservation. Mice injected with larvae which successfully withstood cryopreservation showed a significant reduction in worm burden following cercarial challenge. No protection was achieved in mice which received larvae damaged by a suboptimal thawing rate. Parallel comparison of several humoral and cellular responses in mice which received either inoculum revealed that induction of activated macrophages and production of macrophage-activating lymphokine activity were the strongest correlates to development of protective immunity. Protected mice also showed marginal 30-min skin test reactivity and weak but transient 24-h delayed-type hypersensitivity to a soluble adult worm preparation. In contrast, indistinguishable levels of circulating antibodies to soluble and tegumental antigens developed in the two immunization groups, and antigen-stimulated lymphocyte blastogenic responses were strong and essentially equivalent in magnitude. These studies strongly suggested that in this new model for investigating anti-schistosome effector mechanisms, responses contributing to the development of activated macrophages may be essential for induction of protective immunity.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bickle Q. D., Andrews B. J., Taylor M. G. Schistosoma mansoni: characterization of two protective monoclonal antibodies. Parasite Immunol. 1986 Jan;8(1):95–107. doi: 10.1111/j.1365-3024.1986.tb00836.x. [DOI] [PubMed] [Google Scholar]
  2. Boros D. L., Warren K. S. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J Exp Med. 1970 Sep 1;132(3):488–507. doi: 10.1084/jem.132.3.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Byram J. E., von Lichtenberg F., Lewis F. A., Stirewalt M. A. Pathology of a live attenuated anti-schistosome vaccine in mice. Am J Trop Med Hyg. 1983 Jan;32(1):94–105. doi: 10.4269/ajtmh.1983.32.94. [DOI] [PubMed] [Google Scholar]
  4. Ch'ang L. Y., Colley D. G. Cutaneous sensitivity induced by immunization with irradiated Schistosoma mansoni cercariae. II. Autoimmunoregulation of cell-mediated cutaneous sensitivity and its reversal. Cell Immunol. 1986 Jun;100(1):129–139. doi: 10.1016/0008-8749(86)90013-4. [DOI] [PubMed] [Google Scholar]
  5. Colley D. G., Wikel S. K. Schistosoma mansoni: simplified method for the production of schistosomules. Exp Parasitol. 1974 Feb;35(1):44–51. doi: 10.1016/0014-4894(74)90005-8. [DOI] [PubMed] [Google Scholar]
  6. Correa-Oliveira R., Sher A. Defective immunoglobulin M responses to vaccination or infection with Schistosoma mansoni in xid mice. Infect Immun. 1985 Nov;50(2):409–414. doi: 10.1128/iai.50.2.409-414.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Correa-Oliveira R., Sher A., James S. L. Defective vaccine-induced immunity to Schistosoma mansoni in P strain mice. I. Analysis of antibody responses. J Immunol. 1984 Sep;133(3):1581–1586. [PubMed] [Google Scholar]
  8. Dean D. A., Bukowski M. A., Clark S. S. Attempts to transfer the resistance of Schistosoma mansoni-infected and irradiated cercaria-immunized mice by means of parabiosis. Am J Trop Med Hyg. 1981 Jan;30(1):113–120. doi: 10.4269/ajtmh.1981.30.113. [DOI] [PubMed] [Google Scholar]
  9. Dean D. A., Mangold B. L., Georgi J. R., Jacobson R. H. 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. Am J Trop Med Hyg. 1984 Jan;33(1):89–96. doi: 10.4269/ajtmh.1984.33.89. [DOI] [PubMed] [Google Scholar]
  10. Dean D. A. Schistosoma and related genera: acquired resistance in mice. Exp Parasitol. 1983 Feb;55(1):1–104. doi: 10.1016/0014-4894(83)90002-4. [DOI] [PubMed] [Google Scholar]
  11. Deelder A. M., Kornelis D., Makbin M., Noordpool H. N., Codfried R. M., Rotmans J. P., Oostburg B. F. Applicability of different antigen preparations in the enzyme-linked immunosorbent assay for schistosomiasis mansoni. Am J Trop Med Hyg. 1980 May;29(3):401–410. doi: 10.4269/ajtmh.1980.29.401. [DOI] [PubMed] [Google Scholar]
  12. Greene M. I., Benacerraf B. Studies on hapten specific T cell immunity and suppression. Immunol Rev. 1980;50:163–186. doi: 10.1111/j.1600-065x.1980.tb00311.x. [DOI] [PubMed] [Google Scholar]
  13. Hayunga E. G., Murrell K. D., Taylor D. W., Vannier W. E. Isolation and characterization of surface antigens from Schistosoma mansoni. I. Evaluation of techniques for radioisotope labeling of surface proteins from adult worms. J Parasitol. 1979 Aug;65(4):488–496. [PubMed] [Google Scholar]
  14. James E. R. Schistosoma mansoni: cryopreservation of schistosomula by two-step addition of ethanediol and rapid cooling. Exp Parasitol. 1981 Aug;52(1):105–116. doi: 10.1016/0014-4894(81)90066-7. [DOI] [PubMed] [Google Scholar]
  15. James S. L., Correa-Oliveira R., Leonard E. J. Defective vaccine-induced immunity to Schistosoma mansoni in P strain mice. II. Analysis of cellular responses. J Immunol. 1984 Sep;133(3):1587–1593. [PubMed] [Google Scholar]
  16. James S. L. Induction of protective immunity against Schistosoma mansoni by a nonliving vaccine. III. Correlation of resistance with induction of activated larvacidal macrophages. J Immunol. 1986 May 15;136(10):3872–3877. [PubMed] [Google Scholar]
  17. James S. L., Labine M., Sher A. 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. Cell Immunol. 1981 Nov 15;65(1):75–83. doi: 10.1016/0008-8749(81)90053-8. [DOI] [PubMed] [Google Scholar]
  18. James S. L., Natovitz P. C., Farrar W. L., Leonard E. J. Macrophages as effector cells of protective immunity in murine schistosomiasis: macrophage activation in mice vaccinated with radiation-attenuated cercariae. Infect Immun. 1984 Jun;44(3):569–575. doi: 10.1128/iai.44.3.569-575.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lewis F. A., Stirewalt M., Leef J. L. Schistosoma mansoni: radiation dose and morphologic integrity of schistosomules as factors for an effective cryopreserved live vaccine. Am J Trop Med Hyg. 1984 Jan;33(1):125–131. doi: 10.4269/ajtmh.1984.33.125. [DOI] [PubMed] [Google Scholar]
  20. Lewis F. A., Wilson E. M. Regional and splenic lymphocyte proliferative responses of mice exposed to normal or irradiated Schistosoma mansoni cercariae. Am J Trop Med Hyg. 1982 May;31(3 Pt 1):505–513. doi: 10.4269/ajtmh.1982.31.505. [DOI] [PubMed] [Google Scholar]
  21. Lewis F. A., Wilson E. M. Schistosoma mansoni: splenic lymphocyte responses of mice after initial exposure to highly irradiated cercariae. Exp Parasitol. 1982 Aug;54(1):21–32. doi: 10.1016/0014-4894(82)90106-0. [DOI] [PubMed] [Google Scholar]
  22. Mangold B. L., Dean D. A. Passive transfer with serum and IgG antibodies of irradiated cercaria-induced resistance against Schistosoma mansoni in mice. J Immunol. 1986 Apr 1;136(7):2644–2648. [PubMed] [Google Scholar]
  23. Murrell K. D., Clark S., Dean D. A., Vannier W. E. Influence of mouse strain on induction of resistance with irradiated Schistosoma mansoni cercariae. J Parasitol. 1979 Oct;65(5):829–831. [PubMed] [Google Scholar]
  24. Prouvost-Danon A., Javierre M. Q., Lima M. S. Passive anaphylactic reaction in mouse peritoneal mast cells in vitro. Life Sci. 1966 Oct;5(19):1751–1760. doi: 10.1016/0024-3205(66)90050-6. [DOI] [PubMed] [Google Scholar]
  25. Sher A., Correa-Oliveira R., Hieny S., Hussain R. Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. IV. Analysis of the role of IgE antibodies and mast cells. J Immunol. 1983 Sep;131(3):1460–1465. [PubMed] [Google Scholar]
  26. Sher A., Hieny S., James S. L., Asofsky R. 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. J Immunol. 1982 Apr;128(4):1880–1884. [PubMed] [Google Scholar]
  27. Stirewalt M., Lewis F. A., Cousin C. E., Leef J. L. Cryopreservation of schistosomules of Schistosoma mansoni in quantity. Am J Trop Med Hyg. 1984 Jan;33(1):116–124. doi: 10.4269/ajtmh.1984.33.116. [DOI] [PubMed] [Google Scholar]
  28. Walter C. A., James E. R. Ultrastructural appearance of freeze-substituted schistosomula of Schistosoma mansoni frozen by a two-step cooling schedule. Cryobiology. 1981 Apr;18(2):125–132. doi: 10.1016/0011-2240(81)90084-5. [DOI] [PubMed] [Google Scholar]

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