Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-20T02:23:06.822Z Has data issue: false hasContentIssue false
  • English
  • Français

Ultrastructural observations on the in vitro interaction of rat neutrophils with schistosomula of Schistosoma mansoni in the presence of antibody and/or complement

Published online by Cambridge University Press:  06 April 2009

R. N. Incani  and
Diane J. McLaren
R. N. Incani
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

Rat peritoneal neutrophils adhere to schistosomula of Schistosoma mansoni in vitro in the presence of antibody, complement, or both. Ultrastructural studies have demonstrated that cell adherence is not intimate, and that electron-dense secretions are not liberated onto the parasite surface in the manner described for eosinophils. Cytochemical techniques confirm that peroxidase is confined within intracellularly located neutrophil secretion granules. The metabolic burst is shown to operate during Fc-mediated interactions, but since morphological damage depends upon the presence of complement in the system, toxic oxygen products would seem not to be involved in the initiation of surface perturbation. Complement-dependent, neutrophil-mediated schistosomular damage is characterized by vesiculation of the tegumental outer membrane, an increase in density of the tegumental cytoplasm and the eventual development of focal lesions. The cells migrate laterally to push aside damaged surface tissues and then adhere intimately to the exposed musculature. Damage appears earlier when both antibody and complement are present in the system, and this correlates with higher killing efficiency. The frequently observed association of contaminant eosinophils with areas of parasite damage indicates that eosinophils and neutrophils may cooperate to effect schistosomular killing. In the presence of antibody alone, attached neutrophils exhibit intense phagocytic activity towards the antigen-antibody complex formed at the parasite surface. This phenomenon may account for the eventual detachment of cells and lack of significant parasite damage recorded in this system

Type
Research Article
Information
Parasitology , Volume 86 , Issue 2 , April 1983 , pp. 345 - 357
Copyright
Copyright © Cambridge University Press 1983

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

Anwar, A. R. E., Smithers, S. R. & Kay, A. B. (1979). Killing of schistosomula of Schistosoma mansoni coated with antibody and/or complement by human leucocytes in vitro: requirement for complement in preferential killing by eosinophils. Journal of Immunology 122, 628–37.CrossRefGoogle ScholarPubMed
Bainton, D. F. (1973). Sequential degranulation of the two types of polymorphonuclear leukocyte granules during phagocytosis of microorganisms. Journal of Cell Biology 58, 249–64.CrossRefGoogle ScholarPubMed
Bass, D. A. & Szejda, P. (1979). Eosinophils versus neutrophils in host defence. Killing of newborn larvae of Trichinella spiralis by human granulocytes in vitro. Journal of Clinical Investigation 64, 1415–22.CrossRefGoogle ScholarPubMed
Bentley, A. G., Carlisle, A. S. & Phillips, S. M. (1981). Ultrastructual 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 Scholar
Brink, L. H., McLaren, D. J. & Smithers, S. R. (1977). Schistosoma mansoni: a comparative study of artificially transformed schistosomula and schistosomula recovered after cercarial penetration of isolated skin. Parasitology 74, 73–86.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Vadas, M. A., Wasson, D. L., Dessein, A., Hogan, M., Sherry, B., Gleich, G. J. & David, J. R. (1979). Interaction betweenhuman eosinophils and schistosomula of Schistosoma mansoni. II. The mechanism of irreversible eosinophil adherence. Journal of Experimental Medicine 150, 1456–71.CrossRefGoogle Scholar
Caulfield, J. P., Korman, G., Butterworth, A. E., Hogan, M. & David, J. R. (1980). The adherence of human neutrophils and eosinophils to schistosomula: evidence for membrane fusion between cells and parasites. Journal of Cell Biology 86, 46–63.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1972). The effect of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 79–98.CrossRefGoogle ScholarPubMed
Cline, M. J. (1975). The White Cell. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Colley, D. G., Magalhães-Filho, A. & Coelho, R. B. (1972). Immunopathology of dermal reactions induced by Schistosoma mansoni cercariae and cercarial extract. American Journal of Tropical Medicine and Hygiene 21, 558–68.CrossRefGoogle ScholarPubMed
Czarnetzki, B. M. (1978). Eosinophil chemotactic factor release from neutrophils by Nippo strongylus brasiliensis larvae. Nature, London 271, 553–553.CrossRefGoogle Scholar
Davies, C. & Goose, J. (1979). Killing of newly excysted juveniles of Fasciola hepatica in sensitised rats. Parasite Immunology 3, 81–96.CrossRefGoogle Scholar
Gale, R. P. & Zighelboim, J. (1975). Polymorphonuclear leukocytes in antibody-dependent cellular cytotoxicity. Journal of Immunology 114, 1047–51.CrossRefGoogle ScholarPubMed
Glauert, A. M., Oliver, R. C. & Thorne, K. J. I. (1980). The interaction of human eosinophils and neutrophils with non-phagocytosable surfaces: a model for studying cell mediated immunity in schistosomiasis. Parasitology 80, 525–37.CrossRefGoogle Scholar
Grewal, A. S., Rouse, B. T. & Babiuk, L. A. (1976). Mechanisms of resistance to herpes-viruses: a comparison of the effectiveness of different cell types at mediating antibody-dependent cell-mediated cytotoxicity. Infection and Immunity 15, 698–703.CrossRefGoogle Scholar
Grewal, A. S., Rouse, B. T. & Babiuk, L. A. (1980). Mechanisms of recovery from viral infections: destruction of infected cells by neutrophils and complement. Journal of Immunology 124, 312–19.CrossRefGoogle ScholarPubMed
Henson, P. M. (1971). The immunologic release of constituents from neutrophil leukocytes. II. Mechanisms of release during phagocytosis and adherence to non-phagocytosable particles. Journal of Immunology 107, 1547–57.CrossRefGoogle Scholar
Hockley, D. J. & McLaren, D. J. (1975). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercariae to adult worm. International Journal for Parasitology 3, 13–25.CrossRefGoogle Scholar
Incani, R. N. (1981). Immunity to Schistosoma mansoni: in vitro and in vivo studies on the role of the neutrophil in schistosomular killing. Ph.D. thesis, Brunei University, Uxbridge, Middlesex.Google Scholar
Incani, R. N. & McLaren, D. J. (1980). Neutrophil-mediated cytotoxicity to schistosomula of Schistosoma mansoni. In Biochemistry of Parasites and the Host-Parasite Relationship (ed. Van den Bossche, H.), pp. 491–94. Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
Incani, R. N. & McLaren, D. J. (1981). Neutrophil-mediated cytotoxicity to schistosomula of Schistosoma mansoni in vitro: studies on the kinetics of complement and/or antibody-dependent adherence and killing. Parasite Immunology 3, 107–26.CrossRefGoogle ScholarPubMed
Kazura, J. M. & Aikawa, M. (1980). Host defence mechanisms against Trichinella spiralis infection in the mouse: eosinophil-mediated destruction of newborn larvae in vitro. Journal of Immunology 124, 355–61.CrossRefGoogle ScholarPubMed
Klebanoff, S. J. & Clark, R. A. (1978). The Neutrophil: Function and Clinical Disorders. Amsterdam: North Holland Publishing Co.Google Scholar
Lbventhal, R. & Soulsby, E. J. L. (1972). Nitroblue tetrazolium dye reduction as an indicator of lysosomal activity at a larval surface. Journal of Parasitology 58, 1016–17.CrossRefGoogle Scholar
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 Pathology 84, 479–99.Google ScholarPubMed
McLaren, D. J. (1980 a). Schistosoma mansoni: the parasite surface in relation to host immunity. Tropical Medicine Research Studies, Vol. 1, (ed. Brown, K. N.), Chichester, UK: Research Studies Press/John Wiley.Google Scholar
McLaren, D. J. (1980 b). Ultrastructural observations on the interaction between host cells and parasitic helminths. In Biochemistry of Parasites and the Host-Parasite Relationship, (ed. van den Bossche, H.), pp. 85–98. Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
McLaren, D. J. (1982). The role of eosinophils in tropical disease. Seminars in Haematology 19, 100–6.Google ScholarPubMed
McLaren, D. J., Mackenzie, C. D. & Ramalho-Pinto, F. J. (1977). Ultrastructural observations on the in vitro interaction between rat eosinophils and some parasitic helminths (Schistosoma mansoni, Trichinella spiralis and Nippostrongylus brasiliensis). Clinical and Experimental Immunology 30, 105–18.Google 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. & Ramalho-Pinto, F. J. (1979). Eosinophil-mediated killing of schistosomula of Schistosoma mansoni in vitro: synergistic effect of antibody and complement. Journal of Immunology 123, 1431–38.CrossRefGoogle ScholarPubMed
McLaren, D. J., Ramalho-Pinto, F. J. & Smithers, S. R. (1978). Ultrastructural evidence for complement and antibody-dependent damage to schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Parasitology 77, 313–313.CrossRefGoogle ScholarPubMed
Movat, H. Z. (1976). Pathways to allergic inflammation: the sequelae of antigen-antibody complex formation. Federation Proceedings 35, 2435–41.Google ScholarPubMed
Miller, M. L., Stinnett, J. D. & Clark, L. C. (1980). Ultrastructure of tumoricidal peritoneal exudate cells stimulated in vivo by perfluorochemical emulsions. Journal of the Reticuloendothelial Society 27, 105–18.Google ScholarPubMed
Olsson, I. & Venge, P. (1974). Cationic proteins of human granulocytes. II. Separation of the cationic proteins of the granules of leukemic myeloid cells. Blood 44, 235–46.CrossRefGoogle ScholarPubMed
Perez, H., Clegg, J. A. & Smithers, S. R. (1974). Acquired immunity to Schistosoma mansoni in the rat: measurement of immunity by the lung recovery technique. Parasitology 69, 349–59.CrossRefGoogle ScholarPubMed
Ramalho-Pinto, F. J., Gazzinelli, G., Howells, R. E., Mota-Santos, T. A., Figueiredo, E. A. & Pellegrino, J. (1974). Schistosoma mansoni: a defined system for the step-wise transformation of the cercaria to schistosomule in vitro. Experimental Parasitology 36, 360–72.CrossRefGoogle Scholar
Ramalho-Pinto, F. J., McLaren, D. J. & Smithers, S. R. (1978). Complement-mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Journal of Experimental Medicine 147, 147–56.CrossRefGoogle ScholarPubMed
Segal, A. W., Dorling, J. & Coade, S. (1980). Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes. Biochemical and morphological studies. Journal of Cell Biology 85, 42–59.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Vadas, M. A., David, J. R., Butterworth, A., Pisani, N. & Siongok, T. A. (1979). A new method for the purification of human eosinophils and neutrophils, and a comparison of the ability of these cells to damage schistosomula of Schistosoma mansoni. Journal of Immunology 122, 1228–36.CrossRefGoogle Scholar
Weissman, G., Zurier, R. B., Spicler, P. J. & Goldstein, I. M. (1971). Mechanisms of lysosomal enzyme release from leukocytes exposed to immune complexes and other particles. Journal of Experimental Medicine 134, 149–65.CrossRefGoogle Scholar
Zucker-Franklin, D. & Hirsch, J. G. (1964). Electron microscope studies on the degranulation of rabbit peritoneal leukocytes during phagocytosis. Journal of Experimental Medicine 120, 569–76.CrossRefGoogle ScholarPubMed