Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-27T11:29:07.299Z Has data issue: false hasContentIssue false
  • English
  • Français

Killing of schistosomula of Schistosoma mansoni by macrophages: induction by T-cell clone-derived lymphokines and interferon-gamma

Published online by Cambridge University Press:  06 April 2009

C. F. Kubelka ,
A. Ruppel ,
P. H. Krammer  and
D. Gemsa
C. F. Kubelka
Affiliation:
Institute for Immunology and Serology, University of Heidelberg, F.KG.
A. Ruppel
Affiliation:
Institute for Immunology and Serology, University of Heidelberg, F.KG.
P. H. Krammer
Affiliation:
Institute for Immunology and Genetics of the German Cancer Research Center, Heidelberg, F.R.G.
D. Gemsa
Affiliation:
Institute for Immunology and Serology, University of Heidelberg, F.KG.
Get access Rights & Permissions [Opens in a new window]

Summary

The induction of schistosomulicidal activity of peritoneal macrophages by concanavalin A-stimulated supernatants from long-term T-cell clones and by interferon-gamma (IFN-γ) was investigated in detail. Optimal conditions of in vitro macrophage activation by T-cell clone supernatants were established. Macrophages from 13-week S. mansoni-infected mice responded to lymphokine activation as well as resident mnacrophages from uninfecteci mice. IFN-γ was shown to play an essential role in induction of schistosomulicidal macrophage activity: recombinant IFN-γ at high concentration could induce schistosomula killing, and an anti-IFN-γ antiserum inhibited the induction ofschistosomulicidal activity by T-cell clone supernatants. Our data also indicate that macrophage activation could be obtained by IFN-γ in synergy with other lymphokines in the supernatant of long-term T-cell clones. Macrophages from mice injected with T-cell clone supernatants were primed in vivo and triggered to kill schistosomula in vitro in the presence of lipopolysaccharide (LPS). The data demonstrate that lymphokines produced by T-cell clones and, in particular, IFN-γ can participate in the activation of schistosomulicidal macrophages.

Type
Research Article
Information
Parasitology , Volume 92 , Issue 2 , April 1986 , pp. 325 - 336
Copyright
Copyright © Cambridge University Press 1986

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

Bout, D., Joseph, M., David, J. R. & Capron, A. R. (1981). In vitro killing of S. mansoni schistosomula by lymphokine-activated mouse macrophages. Journal of Immunology 121, 1–5.Google Scholar
Butterworth, A. E., Taylor, D. W., Veith, M. C., Vadas, M. A., Dessein, A., Sturrock, R. F. & Wells, E. (1982). Studies on the mechanisms of immunity in human schistosomiasis. Immuno logical Reviews 61, 5–39.CrossRefGoogle ScholarPubMed
Capron, A., Dessaint, J. P., Capron, M. & Bazin, H. (1975). Specific IgE antibodies in immune adherence of normal macrophages to Schistosoma mansoni schistosomules. Nature, London 253, 474–5.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1972). The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 79–98.CrossRefGoogle ScholarPubMed
Gemsa, D., Debatin, K.-M, Kramer, P. H., Kubelka, C., Deimann, W., Kees, U. & Krammer, P. H. (1983). Macrophage-activating factors from different T cell clones induce distinct macrophage functions. Journal of Immunology 131, 833–44.CrossRefGoogle ScholarPubMed
Hamann, U. & Krammer, P. H. (1985). Activation of macrophage tumor cytotoxicity by the synergism of two T cell-derived lymphokines: immune interferon (IFN-γ) and macrophage cytotoxicity inducing factor 2(MC1F2). European Journal of Immunology 15, 18–24.CrossRefGoogle Scholar
James, S. L., Lazdins, J. K., Hieny, S. & Natovitz, P. (1983). Macrophages as effector cells of protective immunity in murine schistosomiasis. VI. T cell-dependent, lymphokine-mecliateci, activation of macrophages in response to Schistosoma mansoni antigens. Journal of immunology 131, 1481–6.CrossRefGoogle Scholar
James, S. L., Leonard, E. J. & Meltzer, M. S. (1982 b). Macrophages as effector cells of protective immunity in murine schistosomiasis. IV. Coincident induction of macrophage activation for extracellular killing of schistosomula and tumor cells. Cellular Immunology 74, 86–96.CrossRefGoogle ScholarPubMed
James, S. L., Sher, A., Lazdins, J. K. & Meltzer, M. S. (1982 a). Macrophages as effector cells of protective immunity in murine schistosomiasis. ii. Killing of newly transformed schistosomula in vitro by macrophages activated as consequence of Shistosoma mansoni infection. Journal of Immunology 128, 1535–40.CrossRefGoogle Scholar
Joseph, M., Capron, A., Butterworth, A. E., Sturrock, R. F. & Houba, V. (1978). Cytotoxicity of human and baboon mononuclear phagocytes against schistosomula in vitro: induction by immune complexes containing IgE and Shistosoma mansoni antigens. Clinical and Experimental Immunology 33, 48–56.Google Scholar
Kassis, A. I., Aikawa, M. & Mahmoud, A. A. F. (1979). Mouse antibody-dependent eosinophil arid macrophage adherence arid damage to sch istosomula of Schistosoma mansoni. Journal of immunology 122, 398–405.CrossRefGoogle Scholar
Kleinschmidt, W. J. & Schultz, R. M. (1982). Similarities of murine gamma interferon and the lymphokine that renders macrophages cytotoxic. Journal of Interferon Research 2, 291–9.CrossRefGoogle ScholarPubMed
Krammer, P. H., Dy, M., Hültner, L., Isakson, P., Kees, U., Lohmann-Matthes, M. -L., Marcucci, F., Michnay, A., Puré, E., Schimpl, A., Staber, F., Vitetta, E. & Waller, M. (1982). Production of lymphokines by murine T cells grown in limiting dilution and long-term cultures. In Isolation, Characterization and Utilization of T Lymphocyte Clones, (ed. Fathman, C. F. and Fitch, F.), pp. 253–262. New York: Academic Press.CrossRefGoogle Scholar
Krammer, P. H., Echtenacher, B., Gems, A. D., Hamann, U., Hültner, L., Kaltmann, B., Kees, U., Kubelka, C. & Marcucci, F. (1983). Immune interferon (IFN-γ), macrophage activating factors (MAFs) and colony stimulating factors (CSFs) secreted by T cell clones in limiting dilution microcultures, longterm cultures and by T cell hybridoma. Immunological Reviews 76, 5–28.CrossRefGoogle Scholar
Mahmoud, A. A. F., Peters, P. A. S., Civil, R. H. & Reminton, J. S. (1979). In vitro killing of schistosomula of Schistosoma mansoni by BCG and C. parvum-activated macrophages. Journal of Immunology 122, 1655–7.CrossRefGoogle ScholarPubMed
Männel, D. N., Dröge, W. & Falk, W. (1985). A combination of soluble helper factors bypasses the requirement for stimulator cells and induces nonspecific cytotoxic T cell responses. Immunobiology 170, 146–57.CrossRefGoogle ScholarPubMed
March, S. C., Parikh, F. & Cuatrecasas, P. (1974). A simplified method for cyanogen bromide activation of agarose for affinity chromatrography. Analytical Biochemistry 60, 149–56.CrossRefGoogle Scholar
Marcucci, F., Waller, M., Kirchner, H. & Krammer, P. H. (1981). Production of immune interferon (TFN-γ) by murine T cell clones from long-term cultures. Nature, London. 29, 79–81.CrossRefGoogle Scholar
Meltzer, M. S. (1981). Macrophage activation for tumor cytotoxicity: characterization of priming and trigger signals during lymphokine activation. Journal of immunology 127, 179–83.CrossRefGoogle ScholarPubMed
Murray, H. W., Rubin, B. Y. & Rothermel, C. D. (1983). Killing of intracellular Leishmania donovani by lymphokine-stimulated human mononuclear phagocytes. Journal of Clinical Investigation 72, 1506–10.CrossRefGoogle ScholarPubMed
Nathan, C. F., Murray, H. W., Wiebe, M. E. & Rubin, B. Y. (1983). Identification of interferon-γ as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. Journal of Experimental Medicine 158, 670–89.CrossRefGoogle ScholarPubMed
Olds, G. R., Ellner, J. J., Kholy, A. E. & Mahmoud, A. A. F. (1981). Monocyte-mediated killing of schistosomula of Schistosoma mansoni: alteration in human schistosomiasis mansoni and tuberculosis. Journal of Immunology 127, 1538–42.CrossRefGoogle ScholarPubMed
Pace, J. L., Russell, S. W., Schreiber, R. D., Altman, A. & Katz, D. H. (1983 a). Macrophage activation: priming activity from a T-celi hybridoma is attributable to interferon-γ. Proceedings of the National Academy of Sciences, USA 80, 3782–6.CrossRefGoogle Scholar
Pace, J. L., Russell, S. W., Tones, B. A., Johnson, H. M. & Gray, P. M. (1983 b). Recombinant mouse γ-interferon induces the priming step in macrophage activation of tumor cell killing. Journal of Immunology 130, 2011–13.CrossRefGoogle ScholarPubMed
Rothermel, C. D., Rubin, B. Y. & Murray, H. V. (1983). γ-Interferon is the factor in lymphokine that activates human macrophages to inhibit intracellular Chlamydia psittaci replication. Journal of Immunology 131, 2542–5.CrossRefGoogle ScholarPubMed
Ruppel, A., Rother, U. & Diesfeld, H. J. (1982). Schistosoma mansoni: development of primary infections in mice genetically deficient or intact in the fifth component of complement. Parasitology 85, 314–23.CrossRefGoogle ScholarPubMed
Ruppel, A., Rother, U., Vongericuten, H. & Diesfeld, H. J. (1983). Schistosoma mansoni: complement activation in human and rodent sera by living parasites of various developmental stages. Parasitology 87, 75–86.CrossRefGoogle ScholarPubMed
Russell, S. W., Doe, W. F. & McIntosh, A. T. (1977). Functional characterization of a stable, noncytolytic stage of macrophage activation in tumor. Journal of Experimental Medicine 146, 1511–20.CrossRefGoogle Scholar
Schreiber, R. D., Pace, J. L., Russell, S. W., Altman, A. & Katz, D. (1983). Macrophage-activating factor produced by a T cell hybricloma: phvsiochemical and biosynthetic resemblance to γ-interferon. Journal of Immunology 131, 826–32.CrossRefGoogle Scholar
Schultz, R. M. & Kleinschmidt, W. J. (1983). Functional identity between murine interferon and macrophage activating factor. Nature, London 305, 239–40.CrossRefGoogle ScholarPubMed
Smithers, S. R. & TERRY, R. J. (1965). The infection of laboratory hosts with cercariae of Shistosoma mansoni and the recovery of the adult worms. Parasilology 55, 695–700.CrossRefGoogle Scholar
Smithers, S. R. & Gammage, K. (1980). Recovery of Shistosoma mansoni from the skin, lungs and hepatic portal system of naive mice and mice previously exposed to S. mansoni: evidence for two phases of parasite attrition in immune mice. Parasitology 80, 289–300.CrossRefGoogle Scholar
Svedersky, L. P., Benton, C. V., Berger, W. H., Rinderknecht, E., Harkins, R. N. & Palladino, M. A. (1984). Biological and antigenic similarities of murine interferon-γ and macro-phage-activating factor. Journal of Experimental Medicine 159, 812–27.CrossRefGoogle Scholar
Weinberg, J. B., Chapman, H. A. JR. & Hibbs, J. B. JR. (1978). Characterization of the effects of endotoxin on macrophage tumor cell killing. Journal of Immunology 121, 72–80.CrossRefGoogle ScholarPubMed