Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-03T05:05:42.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential regulation of murine Mesocestoides corti infection by bacterial lipopolysaccharide and interferon-γ

Published online by Cambridge University Press:  06 April 2009

P. Jenkins ,
J. B. Dixon ,
S. Haywood ,
N. K. Rakha  and
S. D. Carter
P. Jenkins
Affiliation:
Departments of Veterinary PathologyUniversity of Liverpool, P.O. Box 147, Liverpool L69 3BX
J. B. Dixon
Affiliation:
Departments of Veterinary PathologyUniversity of Liverpool, P.O. Box 147, Liverpool L69 3BX
S. Haywood
Affiliation:
Departments of Veterinary PathologyUniversity of Liverpool, P.O. Box 147, Liverpool L69 3BX
N. K. Rakha
Affiliation:
Departments of Veterinary PathologyUniversity of Liverpool, P.O. Box 147, Liverpool L69 3BX
S. D. Carter
Affiliation:
Departments of Veterinary PathologyUniversity of Liverpool, P.O. Box 147, Liverpool L69 3BX Veterinary Clinical Science, University of Liverpool, P.O. Box 147, Liverpool L69 3BX
Get access Rights & Permissions [Opens in a new window]

Summary

Many liver-invasive parasites cause extensive liver damage which may result in an impaired ability to catabolize endotoxin. The influence of endogenous endotoxin on the progress of liver-invasive parasitic diseases has been investigated in murine Mesocestoides corti infection. Invasion of liver tissue by tetrathyridia resulted in extensive parenchymal destruction with fibrosis. In association with this, undetoxified endotoxin, in potentially biologically active concentration, was found on peritoneal macrophages, 5 months post-M. corti infection. Host susceptibility was influenced by the Lps gene for responsiveness to lipopolysaccharide (LPS). The parasite burden of LPS-responsive (C3H/HeN) mice was significantly increased in the livers of these mice when compared to LPS-resistant (C3H/HeJ) mice. LPS reduced the ability of normal peritoneal macrophages to kill tetrathyridia, when co-cultured in vitro. LPS also abrogated the ability of recombinant interferon-γ (r.IFN-γ) to enhance macrophage larvicidal activity. These in vitro findings were confirmed in vivo. Daily intraperitoneal administration of LPS, at low concentration, caused a 4-fold increase in parasite burden in the liver, while r.IFN-γ at optimal concentration reduced parasite burden by 57%. Post-infection macrophages have previously been shown to be refractory to cytokine-activation for larval killing. In this report, we conclude that (1) this refractoriness may be due to the presence of undetoxified endotoxin on post-infection macrophages and (2) endotoxin may reduce host resistance by abrogating effector macrophage response to IFN-γ.

Keywords

Mesocestoides cortiregulationlipopolysaccharideinterferon
Type
Research Article
Information
Parasitology , Volume 102 , Issue 1 , February 1991 , pp. 125 - 132
Copyright
Copyright © Cambridge University Press 1991

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

Beutler, B. & Cerami, A. (1987). Cachectin: more than a tumor necrosis factor. New England Journal of Medicine 316, 379–85.Google Scholar
Blanchard, D. K., Djeu, J. Y., Klein, T. W., Friedman, H. & Stewart, W. E. (1986). Interferon-γ induction by lipopolysaccharide: dependence on interleukin 2 and macrophages. Journal of Immunology 136, 963–70.CrossRefGoogle ScholarPubMed
Bocci, V. (1988). Roles of interferon produced in physiological conditions. A speculative review. Immunology 64, 1–9.Google ScholarPubMed
De Maeyer, E. & De Maeyer-Guignard, J. (1988). Interferons and Other Regulatory Cytokines. New York: John Wiley and Sons.Google Scholar
Felton, S. C., Prior, R. B., Spagna, V. A. & Krier, J. P. (1980). Evaluation of Plasmodium berghei for endotoxin by the Limulus lysate assay. Journal of Parasitology 66, 846–7.CrossRefGoogle ScholarPubMed
Jakobsen, P. H., Baek, L. & Jepsen, S. (1988). Demonstration of soluble Plasmodium falciparum antigens reactive with Limulus amoebocyte lysate and polymixin B. Parasite Immunology 10, 593–606.CrossRefGoogle Scholar
James, S. L., Glaven, J., Goldenberg, S., Meltzer, M. S. & Pearce, E. (1990). Tumour necrosis factor (TNF) as a mediator of macrophage helminthotoxic activity. Parasite Immunology 12, 1–13.CrossRefGoogle ScholarPubMed
Jenkins, P., Dixon, J. B., Rakha, N. K. & Carter, S. D. (1990). Regulation of macrophage-mediated larvicidal activity in Echinococcus granulosus and Mesocestoides corti (Cestoda) infection in mice. Parasitology 100, 309–15.CrossRefGoogle ScholarPubMed
Judson, D. G., Dixon, J. B. & Skerritt, G. C. (1987). Occurrence and biochemical characteristics of cestode lymphocyte mitogens. Parasitology 94, 151–60.CrossRefGoogle ScholarPubMed
Kirchner, H., Weyland, A. & Storch, E. (1986). Local interferon induction by bacterial lipopolysaccharide in mice after pretreatment with Corynebacterium parvum. Journal of Interferon Research 6, 483–9.CrossRefGoogle ScholarPubMed
Kongshavn, P. A. L. & Ghadirian, E. (1988). Enhancing and suppressive effects of tumour necrosis factor/cachectin on growth of Trypanosoma musculi. Parasite Immunology 10, 581–8.Google Scholar
Lammas, D. A., Mitchell, L. A. & Wakelin, D. (1987). Adoptive transfer of enhanced eosinophilia and resistance to infection in mice by an in vitro generated T-cell line specific for Mesocestoides corti larval antigen. Parasite Immunology 9, 591–601.CrossRefGoogle Scholar
Le, J., Lin, J.-X., Henriksen-De Stefano, D. & Vilcek, J. (1986). Bacterial lipopolysaccharide-induced interferon-γ production: roles of interleukin 1 and interleukin 2. Journal of Immunology 136, 4525–30.CrossRefGoogle ScholarPubMed
Loose, L. D., Trejo, R. & Di Luzio, N. R. (1971). Impaired endotoxin detoxification as a factor in enhanced endotoxin sensitivity of malaria infected mice. Proceedings of the Society for Experimental Biology and Medicine 137, 794–7.Google Scholar
Lumsden, A. B., Henderson, M. & Kutner, M. H. (1988). Endotoxin levels measured by a chromogenic assay in portal, hepatic and peripheral venous blood in patients with cirrhosis. Hepatology 8, 232–8.Google Scholar
Mitchell, G. F. & Handman, E. (1977). Studies on immune responses to larval cestodes in mice: a simple mechanism of non-specific immunosuppression in Mesocestoides corti infected mice. Australian Journal of Experimental Biology and Medical Science 55, 615–22.CrossRefGoogle ScholarPubMed
Morris, A. G. & Ward, G. (1987). Production of recombinant interferons by expression in heterologous mammalian cells. In Interferons and Lymphokines: a Practical Approach (ed. Clemens, M., Morris, A. & Gearing, A.), pp. 61–71. Oxford: I.R.L. Press.Google Scholar
Munford, R. S. (1988). Enzymatic deacylation of bacterial lipopolysaccharide by human neutrophils and murine macrophages. In Bacteria–Host Cell Interaction (ed. Horwitz, M. A.)., pp. 123–40. New York: Alan R. Liss, Inc.Google Scholar
Ravin, H. A. & Fine, J. (1962). Biological implications of intestinal endotoxins. Federation Proceedings 21, 65–8.Google ScholarPubMed
Rosenstreich, D. L., Glode, L. M., Wahl, L. M., Sandberg, A. L. & Mergenhagen, S. E. (1977). Analysis of the cellular defects of endotoxin-unresponsive C3H/H1J mice. In Microbiology-1977 (ed. D., Schlessinger), pp. 314–320. Washington DC.: American Society for Microbiology.Google Scholar
Rosenstreich, D. L. & Vogel, S. N. (1980). Central role of macrophages in the host response to endotoxin. In Microbiology-1980 (ed. D., Schlessinger), pp. 11–15. Washington DC.: American Society for Microbiology.Google Scholar
Shirai, M., Yoshimura, A., Nishioka, M., Shiga, J., Mori, W., Fukuda, I. & Kanegasaki, S. (1989). Organ distribution of 3H-endotoxin in rats with liver fibrosis and rats with liver cirrhosis. Hepatogastroenterology 36, 172–4.Google ScholarPubMed
Specht, D. & Widmer, E. A. (1972). Response of mouse liver to infection with tetrathyridia of Mesocestoides (Cestoda). Journal of Parasitology 58, 431–7.CrossRefGoogle ScholarPubMed
Taverne, J., Tavernier, J., Fiers, W. & Playfair, J. H. L. (1987). Recombinant tumour necrosis factor inhibits malaria parasites in vivo but not in vitro. Clinical and Experimental Immunology 67, 1–5.Google Scholar
Tubbs, H. (1980). Endotoxin in human and murine malaria. Transactions of the Royal Society for Tropical Medicine and Hygiene 74, 121–3.Google Scholar
Van-Bossuyt, H., De-Zanger, R. B. & Wisse, E. (1988). Cellular and subcellular distribution of injected lipopolysaccharide in rat liver and its inactivation by bile salts. Journal of Hepatology 7, 325–37.CrossRefGoogle ScholarPubMed
Vogel, S. N. & Rosenstreich, D. L. (1981). LPS-unresponsive mice as a model for analysing lymphokine-induced macrophage differentiation in vitro. In Lymphokines 3 (ed. Pick, E. & Landy, M), pp. 149–180. London: Academic Press.Google Scholar
Yokota, M., Kambayashi, J., Tanaka, T., Tsujinaka, T., Sakon, M. & Mori, T. (1989). A simple turbidimetric time assay of the endotoxin in plasma. Journal of Biochemical and Biophysical Methods 18, 97–104.CrossRefGoogle ScholarPubMed