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Pro- and anti-apoptotic activities of protozoan parasites

Published online by Cambridge University Press:  03 October 2006

F. SCHAUMBURG ,
D. HIPPE ,
P. VUTOVA  and
C. G. K. LÜDER
F. SCHAUMBURG
Affiliation:
Institute for Medical Microbiology, Georg-August-University, Kreuzbergring 57, 37075 Göttingen, Germany
D. HIPPE
Affiliation:
Institute for Medical Microbiology, Georg-August-University, Kreuzbergring 57, 37075 Göttingen, Germany
P. VUTOVA
Affiliation:
Institute for Medical Microbiology, Georg-August-University, Kreuzbergring 57, 37075 Göttingen, Germany
C. G. K. LÜDER
Affiliation:
Institute for Medical Microbiology, Georg-August-University, Kreuzbergring 57, 37075 Göttingen, Germany
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Abstract

During infection, programmed cell death, i.e. apoptosis, is an important effector mechanism of innate and adaptive host responses to parasites. In addition, it fulfils essential functions in regulating host immunity and tissue homeostasis. Not surprisingly, however, adaptation of parasitic protozoa to their hosts also involves modulation or even exploitation of cell death in order to facilitate parasite survival in a hostile environment. During recent years, considerable progress has been made in our understanding of apoptosis during parasitic infections and there is now convincing evidence that apoptosis and its modulation by protozoan parasites has a major impact on the parasite-host interaction and on the pathogenesis of disease. This review updates our current knowledge on the diverse functions apoptosis may fulfil during infections with diverse protozoan parasites including apicomplexans, kinetoplastids and amoebae. Furthermore, we also summarize common mechanistic themes of the pro- and anti-apoptotic activities of protozoan parasites. The diverse and complex effects which parasitic protozoa exert on apoptotic cell death within the host highlight fascinating interactions of parasites and their hosts. Importantly, they also stress the importance of further investigations before the modulation of host cell apoptosis can be exploited to combat parasitic infections.

Keywords

Apoptosissignal transductionparasite-host interactionimmunityimmune evasionprotozoapathogenesis
Type
Research Article
Information
Parasitology , Volume 132 , Supplement S1: Programmed cell death and the protozoan parasite , March 2006 , pp. S69 - S85
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Abbasi, M., Kowalewska-Grochowska, K., Bahar, M. A., Kilani, R. T., Winkler-Lowen, B. and Guilbert, L. J. ( 2003). Infection of placental trophoblasts by Toxoplasma gondii. Journal of Infectious Diseases 188, 608–616.CrossRefGoogle Scholar
Adams, J. M. and Cory, S. ( 2002). Apoptosomes: engines for caspase activation. Current Opinion in Cell Biology 14, 715–720.CrossRefGoogle Scholar
Aga, E., Katschinski, D. M., van Zandbergen, G., Laufs, H., Hansen, B., Müller, K., Solbach, W. and Laskay, T. ( 2002). Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. Journal of Immunology 169, 898–905.CrossRefGoogle Scholar
Ameisen, J. C. ( 1996). The origin of programmed cell death. Science 272, 1278–1279.CrossRefGoogle Scholar
Aoki, M. P., Guinazu, N. L., Pellegrini, A. V., Gotoh, T., Masih, D. T. and Gea, S. ( 2004). Cruzipain, a major Trypanosoma cruzi antigen, promotes arginase-2 expression and survival of neonatal mouse cardiomyocytes. American Journal of Physiology – Cell Physiology 286, C206–C212.CrossRefGoogle Scholar
Artis, D., Speirs, K., Joyce, K., Goldschmidt, M., Caamano, J., Hunter, C. A. and Scott, P. ( 2003). NF-kappa B1 is required for optimal CD4+ Th1 cell development and resistance to Leishmania major. Journal of Immunology 170, 1995–2003.CrossRefGoogle Scholar
Ashkenazi, A. and Dixit, V. M. ( 1999). Apoptosis control by death and decoy receptors. Current Opinion in Cell Biology 11, 255–260.CrossRefGoogle Scholar
Beere, H. M. and Green, D. R. ( 2001). Stress management – heat shock protein-70 and the regulation of apoptosis. Trends in Cell Biology 11, 6–10.CrossRefGoogle Scholar
Benedict, C. A., Norris, P. S. and Ware, C. F. ( 2002). To kill or be killed: viral evasion of apoptosis. Nature Immunology 3, 1013–1018.CrossRefGoogle Scholar
Berninghausen, O. and Leippe, M. ( 1997). Necrosis versus apoptosis as the mechanism of target cell death induced by Entamoeba histolytica. Infection and Immunity 65, 3615–3621.Google Scholar
Bertho, A. L., Santiago, M. A., Da Cruz, A. M. and Coutinho, S. G. ( 2000). Detection of early apoptosis and cell death in T CD4+ and CD8+ cells from lesions of patients with localized cutaneous leishmaniasis. Brazilian Journal of Medical and Biological Research 33, 317–325.CrossRefGoogle Scholar
Boettner, D. R., Huston, C. D., Sullivan, J. A. and Petri, W. A. Jr. ( 2005). Entamoeba histolytica and Entamoeba dispar utilize externalized phosphatidylserine for recognition and phagocytosis of erythrocytes. Infection and Immunity 73, 3422–3430.CrossRefGoogle Scholar
Bouillet, P. and Strasser, A. ( 2002). BH3-only proteins – evolutionary conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death. Journal of Cell Science 115, 1567–1574.Google Scholar
Boyer, M. H., Hoff, R., Kipnis, T. L., Murphy, E. D. and Roths, J. B. ( 1983). Trypanosoma cruzi: susceptibility in mice carrying mutant gene lpr (lymphoproliferation). Parasite Immmunology 5, 135–142.CrossRefGoogle Scholar
Bruey, J.-M., Ducasse, C., Bonniaud, P., Ravagnan, L., Susin, S. A., Diaz-Latoud, C., Gurbuxani, S., Arrigo, A.-P., Kroemer, G., Solary, E. and Garrido, C. ( 2000). Hsp27 negatively regulates cell death by interacting with cytochrome c. Nature Cell Biology 2, 645–652.CrossRefGoogle Scholar
Carmen, J. C., Hardi, L. and Sinai, A. P. ( 2006). Toxoplasma gondii inhibits ultraviolet light-induced apoptosis through multiple interactions with the mitochondrion-dependent programmed cell death pathway. Cellular Microbiology 8, 301–315.CrossRefGoogle Scholar
Channon, J. Y., Meselis, K. A., Minns, L. A., Dutta, C. and Kasper, L. H. ( 2002). Toxoplasma gondii induces granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor secretion by human fibroblasts: implications for neutrophil apoptosis. Infection and Immunity 70, 6048–6057.CrossRefGoogle Scholar
Chen, L., Rao, K. V., He, Y. X. and Ramaswamy, K. ( 2002). Skin-stage schistosomula of Schistosoma mansoni produce an apoptosis-inducing factor that can cause apoptosis of T cells. Journal of Biological Chemistry 277, 34329–34335.CrossRefGoogle Scholar
Chen, X. M., Gores, G. J., Paya, C. V. and LaRusso, N. F. ( 1999). Cryptosporidium parvum induces apoptosis in biliary epithelia by a Fas/Fas ligand-dependent mechanism. American Journal of Physiology 277, G599–G608.CrossRefGoogle Scholar
Chen, X. M., Levine, S. A., Splinter, P. L., Tietz, P. S., Ganong, A. L., Jobin, C., Gores, G. J., Paya, C. V. and LaRusso, N. F. ( 2001). Cryptosporidium parvum activates nuclear factor kappaB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 120, 1774–1783.CrossRefGoogle Scholar
Chuenkova, M. V., Furnari, F. B., Cavenee, W. K. and Pereira, M. A. ( 2001). Trypanosoma cruzi trans-sialidase: a potent and specific survival factor for human Schwann cells by means of phosphatidylinositol 3-kinase/Akt signaling. Proceedings of the National Academy of Sciences, USA 98, 9936–9941.CrossRefGoogle Scholar
Chuenkova, M. V. and Pereira, M. A. ( 2000). A trypanosomal protein synergizes with the cytokines ciliary neurotrophic factor and leukemia inhibitory factor to prevent apoptosis of neuronal cells. Molecular Biology of the Cell 11, 1487–1498.CrossRefGoogle Scholar
Chwieralski, C. E., Welte, T. and Buhling, F. ( 2006). Cathepsin-regulated apoptosis. Apoptosis 11, 143–149.CrossRefGoogle Scholar
Cory, S., Huang, D. C. S. and Adams, J. M. ( 2003). The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22, 8590–8607.CrossRefGoogle Scholar
Cummings, J., Ward, T. H., Ranson, M. and Dive, C. ( 2004). Apoptotic pathways-targeted drugs-from the bench to the clinic. Biochimica et Biophysica Acta 1705, 53–66.Google Scholar
Das, G., Vohra, H., Rao, K., Saha, B. and Mishra, G. C. ( 1999). Leishmania donovani infection of a susceptible host results in CD4+ T-cell apoptosis and decreased Th1 cytokine production. Scandinavian Journal of Immunology 49, 307–310.CrossRefGoogle Scholar
Denkers, E. Y., Yap, G., Scharton-Kersten, T., Charest, H., Butcher, B., Caspar, P., Hieny, S. and Sher, A. ( 1997). Perforin-mediated cytolysis plays a limited role in host resistance to Toxoplasma gondii. Journal of Immunology 159, 1903–1908.Google Scholar
Deponte, M. and Becker, K. ( 2004). Plasmodium falciparum – do killers commit suicide? Trends in Parasitology 20, 165–169.Google Scholar
Desbarats, J., Stone, J. E., Lin, L., Zakeri, Z. F., Davis, G. S., Pfeiffer, L. M., Titus, R. G. and Newell, M. K. ( 2000). Rapid early onset lymphocyte cell death in mice resistant, but not susceptible to Leishmania major infection. Apoptosis 5, 189–196.CrossRefGoogle Scholar
Dessauge, F., Hilaly, S., Baumgartner, M., Blumen, B., Werling, D. and Langsley, G. ( 2005 b). C-myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene 24, 1075–1083.Google Scholar
Dessauge, F., Lizundia, R. and Langsley, G. ( 2005 a). Constitutively activated CK2 potentially plays a pivotal role in Theileria-induced lymphocyte transformation. Parasitology 130, S37–S44.Google Scholar
Deveraux, Q. L., Takahashi, R., Salvesen, G. S. and Reed, J. C. ( 1997). X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388, 300–304.CrossRefGoogle Scholar
Dobbelaere, D. and Heussler, V. ( 1999). Transformation of leukocytes by Theileria parva and T. annulata. Annual Reviews in Microbiology 53, 1–42.Google Scholar
Dobbelaere, D. A. and Küenzi, P. ( 2004). The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Current Opinion in Immunology 16, 524–530.CrossRefGoogle Scholar
Dockrell, D. H. ( 2003). The multiple roles of Fas ligand in the pathogenesis of infectious diseases. Clinical Microbiology and Infection 9, 766–779.CrossRefGoogle Scholar
Eda, S. and Sherman, I. W. ( 2002). Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine. Cellular Physiology and Biochemistry 12, 373–384.CrossRefGoogle Scholar
Eidsmo, L., Nylen, S., Khamsipour, A., Hedblad, M. A., Chioudi, F. and Akuffo, H. ( 2005). The contribution of the Fas/FasL apoptotic pathway in ulcer formation during Leishmania major-induced cutaneous leishmaniasis. American Journal of Pathology 166, 1099–1108.CrossRefGoogle Scholar
Eidsmo, L., Wolday, D., Berhe, N., Sabri, F., Satti, I., El Hassan, A. M., Sundar, S., Chiodi, F. and Akuffo, H. ( 2002). Alteration of Fas and Fas ligand expression during human visceral leishmaniasis. Clinical and Experimental Immunology 130, 307–313.CrossRefGoogle Scholar
Ekert, P. G., Silke, J. and Vaux, D. L. ( 1999). Caspase inhibitors. Cell Death and Differentiation 6, 1081–1086.CrossRefGoogle Scholar
Everett, H. and McFadden, G. ( 1999). Apoptosis: an innate immune response to virus infection. Trends in Microbiology 7, 160–165.CrossRefGoogle Scholar
Ferri, K. F. and Kroemer, G. ( 2001). Organelle-specific initiation of cell death pathways. Nature Cell Biology 3, E255–E263.CrossRefGoogle Scholar
Freire-de-Lima, C., Nunes, M. P., Corte-Real, S., Soares, M. P., Previato, J. O., Mendonca-Previato, L. and DosReis, G. A. ( 1998). Proapoptotic activity of a Trypanosoma cruzi ceramide-containing glycolopid turned on in host macrophages by IFN-γ. Journal of Immunology 161, 4909–4916.Google Scholar
Freire-de-Lima, C. G., Nascimento, D. O., Soares, M. B. P., Bozza, P. T., Castro-Faria-Neto, H. C., de Mello, F. G., DosReis, G. A. and Lopes, M. F. ( 2000). Uptake of apoptotic cells drives the growth of a pathogenic trypanosome in macrophages. Nature 403, 199–203.CrossRefGoogle Scholar
Gavrilescu, L. C. and Denkers, E. Y. ( 2001). IFN-γ overproduction and high level apoptosis are associated with high but not low virulence Toxoplasma gondii infection. Journal of Immunology 167, 902–909.CrossRefGoogle Scholar
Girard, M., Bisser, S., Courtioux, B., Vermot-Desroches, C., Bouteille, B., Wijdenes, J., Preud'homme, J. L. and Jauberteau, M. O. ( 2003). In vitro induction of microglial and endothelial cell apoptosis by cerebrospinal fluids from patients with human African trypanosomiasis. International Journal for Parasitology 33, 713–720.CrossRefGoogle Scholar
Goddeeris, B. M. and Morrison, W. I. ( 1987). The bovine autologous Theileria mixed leucocyte reaction: influence of monocytes and phenotype of the parasitized stimulator cell on proliferation and parasite specificity. Immunology 60, 63–69.Google Scholar
Goebel, S., Gross, U. and Lüder, C. G. K. ( 2001). Inhibition of host cell apoptosis by Toxoplasma gondii is accompanied by reduced activation of the caspase cascade and alterations of poly(ADP-ribose) polymerase expression. Journal of Cell Science 114, 3495–3505.Google Scholar
Goebel, S., Lüder, C. G. K. and Gross, U. ( 1999). Invasion by Toxoplasma gondii protects human-derived HL-60 cells from actinomycin D-induced apoptosis. Medical Microbiology and Immunology 187, 221–226.CrossRefGoogle Scholar
Haase, R., Kirschning, C. J., Sing, A., Schröttner, P., Fukase, K., Kusumoto, S., Wagner, H., Heesemann, J. and Ruckdeschel, K. ( 2003). A dominant role of Toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. Journal of Immunology 171, 4294–4303.CrossRefGoogle Scholar
Häcker, G. and Fischer, S. F. ( 2002). Bacterial anti-apoptitic activities. FEMS Microbiology Letters 211, 1–6.Google Scholar
Hashimoto, M., Nakajima-Shimada, J. and Aoki, T. ( 2005). Trypanosoma cruzi posttranscriptionally up-regulates and exploits cellular FLIP for inhibition of death-inducing signal. Molecular Biology of the Cell 16, 3521–3528.CrossRefGoogle Scholar
Helmby, H., Jönsson, G. and Troye-Blomberg, M. ( 2000). Cellular changes and apoptosis in the spleens and peripheral blood of mice infected with blood-stage Plasmodium chabaudi chabaudi AS. Infection and Immunity 68, 1485–1490.CrossRefGoogle Scholar
Hemmer, C. J., Lehr, H. A., Westphal, K., Unverricht, M., Kratzius, M. and Reisinger, E. C. ( 2005). Plasmodium falciparum malaria: reduction of endothelial cell apoptosis in vitro. Infection and Immunity 73, 1764–1770.CrossRefGoogle Scholar
Hengartner, M. O. ( 2000). The biochemistry of apoptosis. Nature 407, 770–776.CrossRefGoogle Scholar
Hernandez, S. and Schwarz de Tarlovsky, S. ( 1999). Arginine decarboxylase in Trypanosoma cruzi, characteristics and kinetic properties. Cellular and Molecular Biology 45, 383–391.Google Scholar
Heussler, V. T., Küenzi, P., Fraga, F., Schwab, R. A., Hemmings, B. A. and Dobbelaere, D. A. E. ( 2001 b). The Akt/PKB pathway is constitutively activated in Theileria-transformed leucocytes, but does not directly control constitutive NF-κB activation. Cellular Microbiology 3, 537–550.Google Scholar
Heussler, V. T., Küenzi, P. and Rottenberg, S. ( 2001 a). Inhibition of apoptosis by intracellular protozoan parasites. International Journal for Parasitology 31, 1166–1176.Google Scholar
Heussler, V. T., Machado, J. Jr., Fernandez, P. C., Botteron, C., Chen, C.-G., Pearse, M. J. and Dobbelaere, D. A. E. ( 1999). The intracellular parasite Theileria parva protects infected T cells from apoptosis. Proceedings of the National Academy of Sciences, USA 96, 7312–7317.CrossRefGoogle Scholar
Heussler, V. T., Rottenberg, S., Schwab, R., Küenzi, P., Fernandez, P. C., McKellar, S., Shiels, B., Chen, Z. J., Orth, K., Wallach, D. and Dobbelaere, D. A. E. ( 2002). Hijacking of the host cell IKK signalosomes by the transforming parasite Theileria. Science 298, 1033–1036.CrossRefGoogle Scholar
Hisaeda, H., Sakai, T., Ishikawa, H., Maekawa, Y., Yasutomo, K., Good, R. A. and Himeno, K. ( 1997). Heat shock protein 65 induced by γδ T cells prevents apoptosis of macrophages and contributes to host defense in mice infected with Toxoplasma gondii. Journal of Immunology 159, 2375–2381.Google Scholar
Hong, S. J., Dawson, T. M. and Dawson, V. L. ( 2004). Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends in Pharmacological Science 25, 259–264.CrossRefGoogle Scholar
Hsu, L.-C., Park, J. M., Zhang, K., Luo, J.-L., Maeda, S., Kaufman, R. J., Eckmann, L., Guiney, D. G. and Karin, M. ( 2004). The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Science 428, 341–345.CrossRefGoogle Scholar
Hu, M. S., Schwartzman, J. D., Yeaman, G. R., Collins, J., Seguin, R., Khan, I. A. and Kasper, L. H. ( 1999). Fas-FasL interaction involved in pathogenesis of ocular toxoplasmosis in mice. Infection and Immunity 67, 928–935.Google Scholar
Huston, C. D., Boettner, D. R., Miller-Sims, V. and Petri, W. A. Jr. ( 2003). Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infection and Immunity 71, 964–972.CrossRefGoogle Scholar
Huston, C. D., Houpt, E. R., Mann, B. J., Hahn, C. S. and Petri, W. A. Jr. ( 2000). Caspase 3-dependent killing of host cells by the parasite Entamoeba histolytica. Cellular Microbiology 2, 617–625.CrossRefGoogle Scholar
Ishikawa, H., Hisaeda, H., Taniguchi, M., Nakayama, T., Sakai, T., Maekawa, Y., Nakano, Y., Zhang, M., Nishitani, M., Takashima, M. and Himeno, K. ( 2000). CD4(+) v(alpha)14 NKT cells play a crucial role in an early stage of protective immunity against infection with Leishmania major. International Immunology 12, 1267–1274.CrossRefGoogle Scholar
Jäättelä, M. and Tschopp, J. ( 2003). Caspase-independent cell death in T lymphocytes. Nature Immunology 4, 416–423.CrossRefGoogle Scholar
James, E. R. and Green, D. R. ( 2004). Manipulation of apoptosis in the host-parasite interaction. Trends in Parasitology 20, 280–287.CrossRefGoogle Scholar
Jenson, J. S., O'Connor, R., Osborne, J. and Devaney, E. ( 2002). Infection with Brugia microfilariae induces apoptosis of CD4(+) T lymphocytes: a mechanism of immune unresponsiveness in filariasis. European Journal of Immunology 32, 858–867.3.0.CO;2-E>CrossRefGoogle Scholar
Kanaly, S. T., Nashleanas, M., Hondowicz, B. and Scott, P. ( 1999). TNF receptor p55 is required for elimination of inflammatory cells following control of intracellular pathogens. Journal of Immunology 163, 3883–3889.Google Scholar
Keller, P., Schaumburg, F., Fischer, S. F., Häcker, G., Groß, U. and Lüder, C. G. K. ( 2006). Direct inhibition of cytochrome c-induced caspase activation in vitro by Toxoplasma gondii reveals novel mechanisms of interference with host cell apoptosis. FEMS Microbiological Letters 258, 312–319.CrossRefGoogle Scholar
Kern, P., Dietrich, M., Hemmer, C. and Wellinghausen, N. ( 2000). Increased levels of soluble Fas ligand in serum in Plasmodium falciparum malaria. Infection and Immunity 68, 3061–3063.CrossRefGoogle Scholar
Khan, I. A., Matsuura, T. and Kasper, L. H. ( 1996). Activation-mediated CD4+ T cell unresponsiveness during acute Toxoplasma gondii infection in mice. International Immunology 8, 887–896.CrossRefGoogle Scholar
Krammer, P. H. ( 2000). CD95's deadly mission in the immune system. Nature 407, 789–795.CrossRefGoogle Scholar
Küenzi, P., Schneider, P. and Dobbelaere, D. A. ( 2003). Theileria parva-transformed T cells show enhanced resistance to Fas/Fas ligand-induced apoptosis. Journal of Immunology 171, 1224–1231.CrossRefGoogle Scholar
Leiriao, P., Albuquerque, S. S., Corso, S., van Gemert, G.-J., Sauerwein, R. W., Rodriguez, A., Giordano, S. and Mota, M. M. ( 2005). HGF/MET signalling protects Plasmodium-infected host cells from apoptosis. Cellular Microbiology 7, 603–609.CrossRefGoogle Scholar
Li, E., Becker, A. and Stanley, S. L. Jr. ( 1989). Chinese hamster ovary cells deficient in N-acetylgalactosaminyltransferase I activity are resistant to Entamoeba histolytica-mediated cytotoxicity. Infection and Immunity 57, 8–12.Google Scholar
Lieberman, J. ( 2003). The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nature Reviews Immunology 3, 361–370.CrossRefGoogle Scholar
Liesenfeld, O., Kosek, J. C. and Suzuki, Y. ( 1997). Gamma interferon induces Fas-dependent apoptosis of Peyer's patch T cells in mice following peroral infection with Toxoplasma gondii. Infection and Immunity 65, 4682–4689.Google Scholar
Lizundia, R., Sengmanivong, L., Guergnon, J., Müller, T., Schnelle, T., Langsley, G. and Shorte, S. L. ( 2005). Use of micro-rotation imaging to study JNK-mediated cell survival in Theileria parva-infected B-lymphocytes. Parasitology 130, 629–635.CrossRefGoogle Scholar
Lopes, M. F., da Veiga, V. F., Santos, A. R., Fonesca, M.-E. F. and DosReis, G. A. ( 1995). Activation-induced CD4+ T cell death by apoptosis in experimental Chagas' disease. Journal of Immunology 154, 744–752.Google Scholar
Lopes, M. F., Nunes, M. P., Henriques-Pons, A., Giese, N., Morse III, H. C., Davidson, W. F., Araújo-Jorge, T. C. and DosReis, G. A. ( 1999). Increased susceptibility of Fas ligand-deficient gld mice to Trypanosoma cruzi infection due to a Th2-biased host immune response. European Journal of Immunology 29, 81–89.3.0.CO;2-Y>CrossRefGoogle Scholar
Lüder, C. G. K. and Gross, U. ( 2005). Apoptosis and its modulation during infection with Toxoplasma gondii: molecular mechanisms and role in pathogenesis. In Role of Apoptotsis in Infection ( ed. Griffin, D. E.), pp. 219–238. Springer-Verlag, Berlin Heidelberg.CrossRef
Lüder, C. G. K., Gross, U. and Lopes, M. F. ( 2001). Intracellular protozoan parasites and apoptosis: diverse strategies to modulate parasite-host interactions. Trends in Parasitology 17, 480–486.CrossRefGoogle Scholar
Martins, G. A., Vieira, L. Q., Cunha, F. Q. and Silva, J. S. ( 1999). Gamma interferon modulates CD95 (Fas) and CD95 ligand (Fas-L) expression and nitric oxide-induced apoptosis during the acute phase of Trypanosoma cruzi infection: a possible role in immune response control. Infection and Immunity 67, 3864–3871.Google Scholar
Matsumoto, J., Kawai, S., Terao, K., Kirinoki, M., Yasutomi, Y., Aikawa, M. and Matsuda, H. ( 2000). Malaria infection induces rapid elevation of the soluble Fas ligand level in serum and subsequent T lymphocytopenia: possible factors responsible for the differences in susceptibility of two species of Macaca monkeys to Plasmodium coatneyi infection. Infection and Immunity 68, 1183–1188.CrossRefGoogle Scholar
McCole, D. F., Eckmann, L., Laurent, F. and Kagnoff, M. F. ( 2000). Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infection and Immunity 68, 1710–1713.CrossRefGoogle Scholar
Mele, R., Gomez Morales, M. A., Tosini, F. and Pozio, E. ( 2004). Cryptospridium parvum at different developmental stages modulates host cell apoptosis in vitro. Infection and Immunity 72, 6061–6067.CrossRefGoogle Scholar
Molestina, R. E., Payne, T. M., Coppens, I. and Sinai, A. P. ( 2003). Activation of NF-κB by Toxoplasma gondii correlates with increased expression of antiapoptotic genes and localization of phosphorylated IκB to the parasitophorous vacuole membrane. Journal of Cell Science 116, 4359–4371.CrossRefGoogle Scholar
Molestina, R. E. and Sinai, A. P. ( 2005). Detection of a novel parasite kinase activity at the Toxoplasma gondii parasitophorous vacuole membrane capable of phosphorylating host IκBα. Cellular Microbiology 7, 351–362.CrossRefGoogle Scholar
Moore, K. J. and Matlashewski, G. ( 1994). Intracellular infection by Leishmania donovani inhibits macrophage inhibits macrophage apoptosis. Journal of Immunology 152, 2930–2937.Google Scholar
Mordue, D. G., Monroy, F., La Regina, M., Dinarello, C. A. and Sibley, L. D. ( 2001). Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. Journal of Immunology 167, 4574–4584.CrossRefGoogle Scholar
Morrison, W. I., Buscher, G., Murray, M., Emery, D. L., Masake, R. A., Cook, R. H. and Wells, P. W. ( 1981). Theileria parva: kinetics of infection in the lymphoid system of cattle. Experimental Parasitology 52, 248–260.CrossRefGoogle Scholar
Nash, P. B., Purner, M. B., Leon, R. P., Clarke, P., Duke, R. C. and Curiel, T. J. ( 1998). Toxoplasma gondii-infected cells are resistant to multiple inducers of apoptosis. Journal of Immunology 160, 1824–1830.Google Scholar
Nelson, B. H. and Willerford, D. M. ( 1998). Biology of the interleukin-2 receptor. Advances in Immunology 70, 1–81.CrossRefGoogle Scholar
Nicholson, D. W. ( 2000). From bench to clinic with apoptosis-based therapeutic agents. Nature 407, 810–816.CrossRefGoogle Scholar
Nickell, S. P. and Sharma, D. ( 2000). Trypanosoma cruzi: roles for perforin-dependent and perforin-independent immune mechanisms in acute resistance. Experimental Parasitology 94, 207–216.CrossRefGoogle Scholar
Nunes, M. P., Andrade, R. M., Lopes, M. F. and DosReis, G. A. ( 1998). Activation-induced T cell death exacerbates Trypanosoma cruzi replication in macrophages cocultured with CD4+ T lymphocytes from infected hosts. Journal of Immunology 160, 1313–1319.Google Scholar
Opferman, J. T. and Korsmeyer, S. J. ( 2003). Apoptosis in the development and maintenance of the immune system. Nature Immunology 4, 410–415.CrossRefGoogle Scholar
Orlofsky, A., Somogyi, R. D., Weiss, L. M. and Prystowsky, M. B. ( 1999). The murine antiapoptotic protein A1 is induced in inflammatory macrophages and constitutively expressed in neutrophils. Journal of Immunolgy 163, 412–419.Google Scholar
Orlofsky, A., Weiss, L. M., Kawachi, N. and Prystowsky, M. B. ( 2002). Deficiency in the anti-apoptotic protein A1-a results in a diminished acute inflammatory response. Journal of Immunolgy 168, 1840–1846.CrossRefGoogle Scholar
Payne, T. M., Molestina, R. E. and Sinai, A. P. ( 2003). Inhibition of caspase activation and a requirement for NF-κB function in the Toxoplasma gondii-mediated blockade of host apoptosis. Journal of Cell Science 116, 4345–4358.CrossRefGoogle Scholar
Pino, P., Vouldoukis, I., Dugas, N., Hassani-Loppion, G., Dugas, B. and Mazier, D. ( 2003 a). Redox-dependent apoptosis in human endothelial cells after adhesion of Plasmodium falciparum-infected erythrocytes. Annals of the New York Academy of Science 1010, 582–586.Google Scholar
Pino, P., Vouldoukis, I., Kolb, J. P., Mahmoudi, N., Desportes-Livage, I., Bricaire, F., Danis, M., Dugas, B. and Mazier, D. ( 2003 b). Plasmodium falciparum-infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. Journal of Infectious Diseases 187, 1283–1290.Google Scholar
Ravdin, J. L., Moreau, F., Sullivan, J. A., Petri, W. A. Jr. and Mandell, G. L. ( 1988). Relationship of the free intracellular calcium to the cytolytic activity of Entamoeba histolytica. Infection and Immunity 56, 1505–1512.Google Scholar
Rawal, S., Majumdar, S. and Vohra, H. ( 2005). Activation of MAPK kinase pathway by Gal/GalNac adherence lectin of E. histolytica: gateway to host response. Molecular and Cellular Biochemistry 268, 93–101.Google Scholar
Refaeli, Y., Van Parijs, L., Alexander, S. L. and Abbas, A. K. ( 2002). Interferon gamma is required for activation-induced death of T lymphocytes. Journal of Experimental Medicine 196, 999–1005.CrossRefGoogle Scholar
Riedl, S. J. and Shi, Y. ( 2004). Molecular mechanisms of caspase regulation during apoptosis. Nature Reviews Molecular Cell Biology 5, 897–907.CrossRefGoogle Scholar
Sakai, T., Hisaeda, H., Ishikawa, H., Maekawa, Y., Zhang, M., Nakao, Y., Takeuchi, T., Matsumoto, K., Good, R. A. and Himeno, K. ( 1999). Expression and role of heat-shock protein 65 (HSP65) in macrophages during Trypanosoma cruzi infection: involvement of HSP65 in prevention of apoptosis of macrophages. Microbes and Infection 1, 419–427.CrossRefGoogle Scholar
Salvesen, G. S. and Abrams, J. M. ( 2004). Caspase activation – stepping on the gas or releasing the brakes? Lessons from humans and flies. Oncogene 23, 2774–2784.CrossRefGoogle Scholar
Savill, J. and Fadock, V. ( 2000). Corpse clearance defines the meaning of cell death. Nature 407, 784–788.CrossRefGoogle Scholar
Scaffidi, C., Schmitz, I., Zha, J., Korsmeyer, S. J., Krammer, P. H. and Peter, M. E. ( 1999). Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. Journal of Biological Chemistry 274, 22532–22538.CrossRefGoogle Scholar
Seo, S. R., Chong, S. A., Lee, S. L., Sung, J. Y., Ahn, Y. S., Chung, K. C. and Seo, J. T. ( 2001). Zn2+-induced ERK activation mediated by reactive oxygen species causes cell death in differentiated PC12 cells. Journal of Neurochemistry 78, 600–610.CrossRefGoogle Scholar
Sim, S., Yong, T.-S., Park, S.-J., Im, K., Kong, Y., Ryu, J.-S., Min, D.-Y. and Shin, M. H. ( 2005). NADPH oxidase-derived reactive oxygen species-mediated activation of ERK1/2 is required for apoptosis of human neutrophils induced by Entamoeba histolytica. Journal of Immunology 174, 4279–4288.CrossRefGoogle Scholar
Simbulan-Rosenthal, C. M., Rosenthal, D. S., Iyer, S., Boulares, A. H. and Smulson, M. E. ( 1998). Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. Journal of Biological Chemistry 273, 13703–13712.CrossRefGoogle Scholar
Song, G., Ouyang, G. and Bao, S. ( 2005). The activation of Akt/PKB signaling pathway and cell survival. Journal of Cellular and Molecular Medicine 9, 59–71.CrossRefGoogle Scholar
Stiles, J. K., Whittaker, J., Sarfo, B. Y., Thompson, W. E., Powell, M. D. and Bond, V. C. ( 2004). Trypanosome apoptotic factor mediates apoptosis in human brain vascular endothelial cells. Molecular and Biochemical Parasitology 133, 229–240.CrossRefGoogle Scholar
Tibbetts, M. D., Zheng, L. and Lenardo, M. J. ( 2003). The death effector domain protein family: regulators of cellular homeostasis. Nature Immunology 4, 404–409.CrossRefGoogle Scholar
Toure-Balde, A., Aribot, G., Tall, A., Spiegel, A. and Roussilhon, C. ( 2000). Apoptosis modulation in mononuclear cells recovered from individuals exposed to Plasmodium falciparum infection. Parasite Immunology 22, 307–318.CrossRefGoogle Scholar
Toure-Balde, A., Sarthou, J. L. and Roussilhon, C. ( 1995). Acute Plasmodium falciparum infection is associated with increased percentages of apoptotic cells. Immunological Letters 46, 196–200.Google Scholar
Trambas, C. M. and Griffiths, G. M. ( 2003). Delivering the kiss of death. Nature Immunology 4, 399–403.CrossRefGoogle Scholar
Wang, K. K. W. ( 2000). Calpain and caspase: can you tell the difference? Trends in Neuroscience 23, 20–26.Google Scholar
Welburn, S. C., Barcinski, M. A. and Williams, G. T. ( 1997). Programmed cell death in trypanosomatids. Parasitology Today 13, 22–26.CrossRefGoogle Scholar
Williams, G. T. ( 1994). Programmed cell death: a fundamental protective response to pathogens. Trends in Microbiology 2, 463–464.CrossRefGoogle Scholar
Van de Sand, C., Horstmann, S., Schmidt, A., Sturm, A., Bolte, S., Krueger, A., Lütgehetmann, M., Pollok, J.-M., Libert, C. and Heussler, V. T. ( 2005). The liver stage of Plasmodium berghei inhibits host cell apoptosis. Molecular Microbiology 58, 731–742.CrossRefGoogle Scholar
Van Dijk, M. R., Douradinha, B., Franke-Fayard, B., Heussler, V., van Dooren, M. W., van Schaijk, B., van Gemert, G. J., Sauerwein, R. W., Mota, M. M., Waters, A. P. and Janse, C. J. ( 2005). Genetically attenuated, P36p-deficient malaria sporozoites induce protective immunity and apoptosis of infected liver cells. Proceedings of the National Acadamy of Sciences, USA 102, 12194–12199.CrossRefGoogle Scholar
Van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W. and Laskay, T. ( 2004). Cutting edge: Neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. Journal of Immunology 173, 6521–6525.CrossRefGoogle Scholar
Zuniga, E., Motran, C. C., Montes, C. L., Yagita, H. and Gruppi, A. ( 2002). Trypanosoma cruzi infection selectively renders parasite-specific IgG+ B lymphocytes susceptible to Fas/Fas ligand-mediated fratricide. Journal of Immunology 168, 3965–3973.CrossRefGoogle Scholar