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. 1976 Sep;84(3):479–500.

Eosinophil-enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni.

F Lichtenberg, A Sher, N Gibbons, B L Doughty
PMCID: PMC2032531  PMID: 961823

Abstract

Exposure of the mouse skin to Schistosoma mansoni cercariae gives rise to acute, exudative inflammation in both normal and immune mice, but the immune response is anamnestically accelerated and is oesinophil-enriched, thereby enhancing opportunities for tegumental contact of schistosomula with host leukocytes, particularly with eosinophils. Many of the inflammatory changes occurring within the first 48 hours after exposure are due to cercarial products, e.g., "penetration tracts," but some remain demonstrable when schistosomula metamorphosed in vitro are injected intradermally and are therefore directed against the schistosomula themselves, such as the leukocyte "streaming patterns" seen in their pathways. In contrast to earlier observations in primates, cellular responses to schistosomula in the mouse lung 4 days after penetration are minimal in either normal or immune mice. Thus, immune cellular responses to schistosomula in mice are limited to an early time period after cercarial penetration and are morphologically suggestive of an antibody-mediated response rather than of delayed hypersensitivity. Our observations complement earlier evidence suggesting that antibody-mediated host leukocyte contact with schistosomula initiates the killing of challenge parasites in immune mice, with the eosinophil probably playing a crucial role.

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Selected References

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

  1. Asherson G. L., Ptak W. Contact and delayed hypersensitivity in the mouse. I. Active sensitization and passive transfer. Immunology. 1968 Sep;15(3):405–416. [PMC free article] [PubMed] [Google Scholar]
  2. Butterworth A. E., Sturrock R. F., Houba V., Rees P. H. Antibody-dependent cell-mediated damage to schistosomula in vitro. Nature. 1974 Dec 6;252(5483):503–505. doi: 10.1038/252503a0. [DOI] [PubMed] [Google Scholar]
  3. Capron A., Capron M., Dupas H., Bout D., Petitprez A. Etude in vitro des phénomènes immunologiques dans la schistosomiase humaine et expérimentale. I. Etude comparative in vitro de l'activité léthale d'immunsérums sur les formes immatures et sur les adultes de Schistosoma mansoni. Int J Parasitol. 1974 Dec;4(6):613–623. doi: 10.1016/0020-7519(74)90026-5. [DOI] [PubMed] [Google Scholar]
  4. Capron A., Dessaint J. P., Capron M., Bazin H. Specific IgE antibodies in immune adherence of normal macrophages to Schistosoma mansoni schistosomules. Nature. 1975 Feb 6;253(5491):474–475. doi: 10.1038/253474a0. [DOI] [PubMed] [Google Scholar]
  5. Clegg J. A., Smithers S. R. Death of schistosome cercariae during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology. 1968 Feb;58(1):111–128. doi: 10.1017/s0031182000073479. [DOI] [PubMed] [Google Scholar]
  6. Clegg J. A., Smithers S. R., Terry R. J. Acquisition of human antigens by Schistosoma mansoni during cultivation in vitro. Nature. 1971 Aug 27;232(5313):653–654. doi: 10.1038/232653a0. [DOI] [PubMed] [Google Scholar]
  7. Clegg J. A., Smithers S. R. The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. Int J Parasitol. 1972 Mar;2(1):79–98. doi: 10.1016/0020-7519(72)90036-7. [DOI] [PubMed] [Google Scholar]
  8. Colley D. G., Magalhães-Filho A., Coelho R. B. Immunopathology of dermal reactions induced by Schistosoma mansoni cercariae and cercarial extract. Am J Trop Med Hyg. 1972 Sep;21(5):558–568. doi: 10.4269/ajtmh.1972.21.558. [DOI] [PubMed] [Google Scholar]
  9. Dean D. A., Wistar R., Chen P. Immune response of guinea pigs to Schistosoma mansoni. I. In vitro effects of antibody and neutrophils, eosinophils and macrophages on schistosomula. Am J Trop Med Hyg. 1975 Jan;24(1):74–82. doi: 10.4269/ajtmh.1975.24.74. [DOI] [PubMed] [Google Scholar]
  10. Dean D. A., Wistar R., Murrell K. D. Combined in vitro effects of rat antibody and neutrophilic leukocytes on schistosomula of Schistosoma mansoni. Am J Trop Med Hyg. 1974 May;23(3):420–428. doi: 10.4269/ajtmh.1974.23.420. [DOI] [PubMed] [Google Scholar]
  11. Dresden M. H., Asch H. L. Proteolytic enzymes in extracts of Schistosoma mansoni cercariae. Biochim Biophys Acta. 1972 Dec 7;289(2):378–384. doi: 10.1016/0005-2744(72)90089-7. [DOI] [PubMed] [Google Scholar]
  12. Hsü S. Y., Hsü H. F., Penick G. D., Lust G. L., Osborne J. W., Cheng H. F. Mechanism of immunity of schistosomiasis: histopathologic study of lesions elicited in rhesus monkeys during immunizations and challenge with cercariae of Schistosoma japonicum. J Reticuloendothel Soc. 1975 Sep;18(3):167–185. [PubMed] [Google Scholar]
  13. LEWERT R. M., LEE C. L. Studies on the passage of helminth larvae through host tissues. I. Histochemical studies on the extracellular changes caused by penetrating larvae. II. Enzymatic activity of larvae in vitro and in vivo. J Infect Dis. 1954 Jul-Aug;95(1):13–51. doi: 10.1093/infdis/95.1.13. [DOI] [PubMed] [Google Scholar]
  14. LIN S. S., SADUN E. H. Studies on the host parasite relationships to Schistosoma japonicum. V. Reactions in the skin, lungs and liver of normal and immune animals following infection with Schistosoma japonicum. J Parasitol. 1959 Oct;45:549–559. [PubMed] [Google Scholar]
  15. LITT M. Studies in experimental eosinophilia. V. Eosinophils in lynph nodes of guinea pigs following primary antigenic stimulation. Am J Pathol. 1963 May;42:529–549. [PMC free article] [PubMed] [Google Scholar]
  16. Lewert R. M., Hopkins D. R., Mandlowitz S. The role of calcium and magnesium ions in invasiveness of schistosome cercariae. Am J Trop Med Hyg. 1966 May;15(3):314–323. doi: 10.4269/ajtmh.1966.15.314. [DOI] [PubMed] [Google Scholar]
  17. Machado A. J., Gazzinelli G., Pellegrino J., Dias de Silva W. Schistosoma mansoni: the role of the complement C3-activating system in the cercaricidal action of normal serum. Exp Parasitol. 1975 Aug;38(1):20–29. doi: 10.1016/0014-4894(75)90034-x. [DOI] [PubMed] [Google Scholar]
  18. Mahmoud A. A., Warren K. S., Graham R. C., Jr Antieosinophil serum and the kinetics of eosinophilia in Schistosomiasis mansoni. J Exp Med. 1975 Sep 1;142(3):560–574. doi: 10.1084/jem.142.3.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mahmoud A. A., Warren K. S., Peters P. A. A role for the eosinophil in acquired resistance to Schistosoma mansoni infection as determined by antieosinophil serum. J Exp Med. 1975 Oct 1;142(4):805–813. doi: 10.1084/jem.142.4.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McLaren D. J., Clegg J. A., Smithers S. R. Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology. 1975 Feb;70(1):67–75. doi: 10.1017/s0031182000048873. [DOI] [PubMed] [Google Scholar]
  21. Murrell K. D., Dean D. A., Stafford E. E. Resistance to infection with Schistosoma mansoni after immunization with worm extracts or live cercariae: role of cytotoxic antibody in mice and guinea pigs. Am J Trop Med Hyg. 1975 Nov;24(6 Pt 1):955–962. doi: 10.4269/ajtmh.1975.24.955. [DOI] [PubMed] [Google Scholar]
  22. Phillips M., Reid W. A., Bruce J. I., Hedlund K., Colvin R. C., Campbell R., Diggs C. L., Sadun E. H. The cellular and humoral immune response to Schistosoma mansoni infections in inbred rats. I. Mechanisms during initial exposure. Cell Immunol. 1975 Sep;19(1):99–116. doi: 10.1016/0008-8749(75)90295-6. [DOI] [PubMed] [Google Scholar]
  23. STIREWALT M. A. Cercaria vs. schistosomule (Schistosoma mansoni): absence of the pericercarial envelope in vivo and the early physiological and histological metamorphosis of the parasite. Exp Parasitol. 1963 Jun;13:395–406. doi: 10.1016/0014-4894(63)90090-0. [DOI] [PubMed] [Google Scholar]
  24. Sher A., Kusel J. R., Perez H., Clegg J. A. Partial isolation of a membrane antigen which induces the formation of antibodies lethal to schistosomes cultured in vitro. Clin Exp Immunol. 1974 Nov;18(3):357–369. [PMC free article] [PubMed] [Google Scholar]
  25. Sher A., Mackenzie P., Smithers S. R. Decreased recovery of invading parasites from the lungs as a parameter of acquired immunity to schistosomiasis in the mouse. J Infect Dis. 1974 Dec;130(6):626–633. doi: 10.1093/infdis/130.6.626. [DOI] [PubMed] [Google Scholar]
  26. Sher A., Smithers S. R., Mackenzie P. Passive transfer of acquired resistance to Schistosoma mansoni in laboratory mice. Parasitology. 1975 Jun;70(Pt 3):347–357. doi: 10.1017/s0031182000052124. [DOI] [PubMed] [Google Scholar]
  27. Smith M. A., Clegg J. A., Kusel J. R., Webbe G. Lung inflammation in immunity to Schistosoma mansoni. Experientia. 1975 May 15;31(5):595–597. doi: 10.1007/BF01932479. [DOI] [PubMed] [Google Scholar]
  28. Smithers S. R., Terry R. J. The immunology of schistosomiasis. Adv Parasitol. 1969;7:41–93. doi: 10.1016/s0065-308x(08)60434-0. [DOI] [PubMed] [Google Scholar]
  29. Smithers S. R., Terry R. J. The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology. 1965 Nov;55(4):695–700. doi: 10.1017/s0031182000086248. [DOI] [PubMed] [Google Scholar]
  30. VOGEL H., MINNING W. Uber die erworbene Resistenz von Macacus rhesus gegenüber Schistosoma japonicum. Z Tropenmed Parasitol. 1953 Oct;4(4):418–505. [PubMed] [Google Scholar]
  31. Vannier W. E., Fireman B. I., Chestnut R. Y., Murrell K. D. Schistosoma mansoni: immediate hypersensitivity to adult antigens in the rat. Exp Parasitol. 1974 Aug;36(1):45–61. doi: 10.1016/0014-4894(74)90112-x. [DOI] [PubMed] [Google Scholar]
  32. von LICHTENBERG, RITCHIE L. S. Cellular resistance against schistosomula of Schistosoma mansoni in Macaca mulatta monkeys following prolonged infections. Am J Trop Med Hyg. 1961 Nov;10:859–869. doi: 10.4269/ajtmh.1961.10.859. [DOI] [PubMed] [Google Scholar]

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