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An experimental model for fatal malaria due to TNF-α-dependent hepatic damage

Published online by Cambridge University Press:  01 April 2008

E. SEIXAS*
Affiliation:
Instituto Gulbenkian de Ciência, Oeiras, Portugal
P. OLIVEIRA
Affiliation:
Instituto Português de Oncologia, Lisboa, Portugal
J. F. MOURA NUNES
Affiliation:
Instituto Português de Oncologia, Lisboa, Portugal
A. COUTINHO
Affiliation:
Instituto Gulbenkian de Ciência, Oeiras, Portugal
*
*Corresponding author: Instituto Gulbenkian de Ciência, Oeiras, Portugal. Tel: +351 21 446 45 17. Fax: +351 21 440 79 70. E-mail: eseixas@igc.gulbenkian.pt

Summary

While BALB/c mice survive infection with blood stages of Plasmodium chabaudi chabaudi (AS), 70% of DBA/2 mice die by day 9–11 of infection, both strains controlling parasitaemia. We describe here that infection of DBA/2 mice results in extensive, multifocal hepatocyte death. Antibody neutralization of TNF-α prevents both liver damage and death.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Adachi, K., Tsutsui, H., Kashiwamura, S., Seki, E., Nakano, H., Takeuchi, O., Takeda, K., Okumura, K., Van Kaer, L., Okamura, H., Akira, S. and Nakanishi, K. (2001). Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. Journal of Immunology 167, 59285934.Google Scholar
Adachi, K., Tsutsui, H., Seki, E., Nakano, H., Takeda, K., Okumura, K., Van Kaer, L. and Nakanishi, K. (2004). Contribution of CD1d-unrestricted hepatic DX5+NKT cells to liver injury in Plasmodium berghei-parasitized erythrocyte-injected mice. International Immunology 16, 787798.Google Scholar
Anand, A. C. and Puri, P. (2005). Jaundice in malaria. Journal of Gastroenterology and Hepatology 20, 13221332.Google Scholar
Bhalla, A., Suri, V. and Singh, V. (2006). Malarial hepatopathy. Journal of Postgraduate Medicine 52, 315320.Google Scholar
Bouharoun-Tayoun, H., Oeuvray, C., Lunel, F. and Druilhe, P. (1995). Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. Journal of Experimental Medicine 182, 409418.CrossRefGoogle ScholarPubMed
Burt, A., Portmann, B. C. and MacSween, R. N. M. (2002). Pathology of the Liver. 4th Edn.Churchill Livingstone, London.Google Scholar
Casals-Pascual, C., Kai, O., Cheung, J. O., Williams, S., Lowe, B., Nyanoti, M., Williams, T. N., Maitland, K., Molyneux, M., Newton, C. R., Peshu, N., Watt, S. M. and Roberts, D. J. (2006). Suppression of erythropoiesis in malarial anemia is associated with hemozoin in vitro and in vivo. Blood 108, 25692577.Google Scholar
Clark, I. A. and Chaudhri, G. (1988). Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. British Journal of Haematology 70, 99103.CrossRefGoogle Scholar
Deller, J. J. Jr., Cifarelli, P. S., Berque, S. and Buchanan, R. (1967). Malaria hepatitis. Military Medicine 132, 614620.Google Scholar
Greenwood, B. and Mutabingwa, T. (2002). Malaria in 2002. Nature, London 415, 670672.Google Scholar
Guha, M., Kumar, S., Choubey, V., Maity, P. and Bandyopadhyay, U. (2006). Apoptosis in liver during malaria: role of oxidative stress and implication of mitochondrial pathway. FASEB Journal 20, 12241226.Google Scholar
Helbok, R., Dent, W., Nacher, M., Lackner, P., Treeprasertsuk, S., Krudsood, S., Wilairatana, P., Silachamroon, U., Looareesuwan, S. and Schmutzhard, E. (2005). The use of the multi-organ-dysfunction score to discriminate different levels of severity in severe and complicated Plasmodium falciparum malaria. American Journal of Tropical Medicine and Hygiene 72, 150154.Google Scholar
Hernandez-Valladares, M., Naessens, J., Musoke, A. J., Sekikawa, K., Rihet, P., Ole-Moiyoi, O. K., Busher, P. and Iraqi, F. A. (2006). Pathology of Tnf-deficient mice infected with Plasmodium chabaudi adami 408XZ. Experimental Parasitology 114, 271278.Google Scholar
Joshi, Y. K., Tandon, B. N., Acharya, S. K., Babu, S. and Tandon, M. (1986). Acute hepatic failure due to Plasmodium falciparum liver injury. Liver 6, 357360.CrossRefGoogle ScholarPubMed
Kamijo, R., Le, J., Shapiro, D., Havell, E. A., Huang, S., Aguet, M., Bosland, M. and Vilcek, J. (1993). Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guerin and subsequent challenge with lipopolysaccharide. Journal of Experimental Medicine 178, 14351440.Google Scholar
Kochar, D. K., Agarwal, P., Kochar, S. K., Jain, R., Rawat, N., Pokharna, R. K., Kachhawa, S. and Srivastava, T. (2003). Hepatocyte dysfunction and hepatic encephalopathy in Plasmodium falciparum malaria. Quarterly Journal of Medicine 96, 505512.Google Scholar
Krishna, S., Waller, D. W., Ter Kuile, F., Kwiatkowski, D., Crawley, J., Craddock, C. F., Nosten, F., Chapman, D., Brewster, D., Holloway, P. A. and White, N. J. (1994). Lactic acidosis and hypoglycaemia in children with severe malaria: pathophysiological and prognostic significance. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 6773.Google Scholar
Kwiatkowski, D., Hill, A. V., Sambou, I., Twumasi, P., Castracane, J., Manogue, K. R., Cerami, A., Brewster, D. R. and Greenwood, B. M. (1990). TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336, 12011204.Google Scholar
Lamikanra, A. A., Brown, D., Potocnik, A., Casals-Pascual, C., Langhorne, J. and Roberts, D. J. (2007). Malarial anemia: of mice and men. Blood 110, 1828.CrossRefGoogle ScholarPubMed
Laskin, D. L. and Pendino, K. J. (1995). Macrophages and inflammatory mediators in tissue injury. Annual Review of Pharmacology and Toxicology 35, 655677.Google Scholar
Leist, M., Gantner, F., Bohlinger, I., Germann, P. G., Tiegs, G. and Wendel, A. (1994). Murine hepatocyte apoptosis induced in vitro and in vivo by TNF-alpha requires transcriptional arrest. Journal of Immunology 153, 17781788.CrossRefGoogle ScholarPubMed
Li, C., Sanni, L. A., Omer, F., Riley, E. and Langhorne, J. (2003). Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infection and Immunity 71, 48504856.Google Scholar
Maitland, K. and Newton, C. R. (2005). Acidosis of severe falciparum malaria: heading for a shock? Trends in Parasitology 21, 1116.Google Scholar
McDevitt, M. A., Xie, J., Gordeuk, V. and Bucala, R. (2004). The anemia of malaria infection: role of inflammatory cytokines. Current Hematology Reports 3, 97106.Google Scholar
Miller, K. L., Silverman, P. H., Kullgren, B. and Mahlmann, L. J. (1989). Tumor necrosis factor alpha and the anemia associated with murine malaria. Infection and Immunity 57, 15421546.Google Scholar
Miller, L. H., Baruch, D. I., Marsh, K. and Doumbo, O. K. (2002). The pathogenic basis of malaria. Nature, London 415, 673679.CrossRefGoogle ScholarPubMed
Murthy, G. L., Sahay, R. K., Sreenivas, D. V., Sundaram, C. and Shantaram, V. (1998). Hepatitis in falciparum malaria. Tropical Gastroenterology 19, 152154.Google ScholarPubMed
Naka, T., Tsutsui, H., Fujimoto, M., Kawazoe, Y., Kohzaki, H., Morita, Y., Nakagawa, R., Narazaki, M., Adachi, K., Yoshimoto, T., Nakanishi, K. and Kishimoto, T. (2001). SOCS-1/SSI-1-deficient NKT cells participate in severe hepatitis through dysregulated cross-talk inhibition of IFN-gamma and IL-4 signaling in vivo. Immunity 14, 535545.Google Scholar
Odeh, M. (2001). The role of tumour necrosis factor-alpha in the pathogenesis of complicated falciparum malaria. Cytokine 14, 1118.Google Scholar
Rodriguez-Acosta, A., Finol, H. J., Pulido-Mendez, M., Marquez, A., Andrade, G., Gonzalez, N., Aguilar, I., Giron, M. E. and Pinto, A. (1998). Liver ultrastructural pathology in mice infected with Plasmodium berghei. Journal of Submicroscopic Cytology and Pathology 30, 299307.Google Scholar
Sachs, J. and Malaney, P. (2002). The economic and social burden of malaria. Nature, London 415, 680685.CrossRefGoogle ScholarPubMed
Schlayer, H. J., Laaf, H., Peters, T., Schaefer, H. E. and Decker, K. (1989). Tumor necrosis factor (TNF) mediated lipopolysaccharide (LPS)-elicited neutrophil sticking to sinusoidal endothelial cells in vivo. In Cells of the Hepatic Sinusoid (ed. Wisse, E., Knook, D. L. and Decker, K.), pp. 319324. Kupfer Cell Foundation, Rijswijk, The Netherlands.Google Scholar
Seixas, E. and Ostler, D. (2005). Plasmodium chabaudi chabaudi (AS): differential cellular responses to infection in resistant and susceptible mice. Experimental Parasitology 110, 394405.CrossRefGoogle ScholarPubMed
Shaffer, N., Grau, G. E., Hedberg, K., Davachi, F., Lyamba, B., Hightower, A. W., Breman, J. G. and Phuc, N. D. (1991). Tumor necrosis factor and severe malaria. Journal of Infectious Diseases 163, 96101.Google Scholar
Shen, H. M. and Pervaiz, S. (2006). TNF receptor superfamily-induced cell death: redox-dependent execution. FASEB Journal 20, 15891598.Google Scholar
Shiff, C. (2002). Integrated approach to malaria control. Clinical Microbiology Reviews 15, 278293.Google Scholar
Snow, R. W., Guerra, C. A., Noor, A. M., Myint, H. Y. and Hay, S. I. (2005). The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature, London 434, 214217.Google Scholar
Spooner, C. E., Markowitz, N. P. and Saravolatz, L. D. (1992). The role of tumor necrosis factor in sepsis. Clinical Immunology and Immunopathology 62, S11S17.Google Scholar
Srivastava, A., Khanduri, A., Lakhtakia, S., Pandey, R. and Choudhuri, G. (1996). Falciparum malaria with acute liver failure. Tropical Gastroenterology 17, 172174.Google ScholarPubMed
Trinchieri, G. and Gerosa, F. (1996). Immunoregulation by interleukin-12. Journal of Leukocyte Biology 59, 505511.Google Scholar
Tsutsui, H., Kayagaki, N., Kuida, K., Nakano, H., Hayashi, N., Takeda, K., Matsui, K., Kashiwamura, S., Hada, T., Akira, S., Yagita, H., Okamura, H. and Nakanishi, K. (1999). Caspase-1-independent, Fas/Fas ligand-mediated IL-18 secretion from macrophages causes acute liver injury in mice. Immunity 11, 359367.CrossRefGoogle ScholarPubMed
Tsutsui, H., Matsui, K., Okamura, H. and Nakanishi, K. (2000). Pathophysiological roles of interleukin-18 in inflammatory liver diseases. Immunological Reviews 174, 192209.Google Scholar
Vassalli, P. (1992). The pathophysiology of tumor necrosis factors. Annual Review of Immunology 10, 411452.Google Scholar
Wilairatana, P., Looareesuwan, S. and Charoenlarp, P. (1994). Liver profile changes and complications in jaundiced patients with falciparum malaria. Tropical Medicine and Parasitology 45, 298302.Google Scholar
Yap, G. S. and Stevenson, M. M. (1991). Production of soluble inhibitor of erythropoiesis during Plasmodium chabaudi AS infection in resistant and susceptible mice. Annals of the New York Academy of Sciences 628, 279281.Google Scholar
Yap, G. S. and Stevenson, M. M. (1994). Inhibition of in vitro erythropoiesis by soluble mediators in Plasmodium chabaudi AS malaria: lack of a major role for interleukin 1, tumor necrosis factor alpha, and gamma interferon. Infection and Immunity 62, 357362.Google Scholar