Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-16T08:41:06.625Z Has data issue: false hasContentIssue false

Regulation of host cell survival by intracellular Plasmodium and Theileria parasites

Published online by Cambridge University Press:  03 October 2006

V. HEUSSLER
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Str. 74, 20359 Hamburg, Germany
A. STURM
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Str. 74, 20359 Hamburg, Germany
G. LANGSLEY
Affiliation:
Institut Cochin, U567 INSERM /UMR 8104 CNRS/Fac de Medecine Paris V, Département Maladies Infectieuses, 22 rue Mechain, 75014 Paris, France

Abstract

Plasmodium and Theileria parasites are obligate intracellular protozoa of the phylum Apicomplexa. Theileria infection of bovine leukocytes induces transformation of host cells and infected leukocytes can be kept indefinitely in culture. Theileria-dependent host cell transformation has been the subject of interest for many years and the molecular basis of this unique phenomenon is quite well understood. The equivalent life cycle stage of Plasmodium is the infection of mammalian hepatocytes, where parasites reside for 2–7 days depending on the species. Some of the molecular details of parasite-host interactions in P. berghei-infected hepatocytes have emerged only very recently. Similar to what has been shown for Theileria-infected leukocytes these data suggest that malaria parasites within hepatocytes also protect their host cell from programmed cell death. However, the strategies employed to inhibit host cell apoptotic pathways appear to be different to those used by Theileria. This review discusses similarities and differences at the molecular level of Plasmodium- and Theileria-induced regulation of the host cell survival machinery.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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

Al-Olayan, E. M., Williams, G. T. and Hurd, H. ( 2002). Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito. International Journal for Parasitology 32, 11331143.CrossRefGoogle Scholar
Alessi, D. R., Kozlowski, M. T., Weng, Q.-P., Morrice, N. and Avruch, J. ( 1997). 3-phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Current Biology 8, 6981.Google Scholar
Aly, A. S. and Matuschewski, K. ( 2005). A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. Journal of Expermental Medicine 202, 225230.Google Scholar
Ameyar, M., Wisniewska, M. and Weitzman, J. B. ( 2003). A role for AP-1 in apoptosis: the case for and against. Biochimie 85, 747752.CrossRefGoogle Scholar
Amino, R., Menard, R. and Frischknecht, F. ( 2005). In vivo imaging of malaria parasites--recent advances and future directions. Current Opinion in Microbiology 8, 407414.CrossRefGoogle Scholar
Baumgartner, M., Angelisova, P., Setterblad, N., Mooney, N., Werling, D., Horejsi, V. and Langsley, G. ( 2003). Constitutive exclusion of Csk from Hck-positive membrane microdomains permits Src kinase-dependent proliferation of Theileria-transformed B lymphocytes. Blood 101, 18741881.CrossRefGoogle Scholar
Baumgartner, M., Chaussepied, M., Moreau, M. F., Werling, D., Davis, W. C., Garcia, A. and Langsley, G. ( 2000). Constitutive PI3-K activity is essential for proliferation, but not survival of Theileria parva-transformed B cells. Cellular Microbiology 2, 329339.CrossRefGoogle Scholar
Bosman, G. J., Willekens, F. L. and Werre, J. M. ( 2005). Erythrocyte aging: a more than superficial resemblance to apoptosis? Cellular Physiology and Biochemistry 16, 18.Google Scholar
Carrolo, M., Giordano, S., Cabrita-Santos, L., Corso, S., Vigario, A. M., Silva, S., Leiriao, P., Carapau, D., Armas-Portela, R., Comoglio, P. M., Rodriguez, A. and Mota, M. M. ( 2003). Hepatocyte growth factor and its receptor are required for malaria infection. Nature Medicine 9, 13631369.CrossRefGoogle Scholar
Chaussepied, M., Lallemand, D., Moreau, M. F., Adamson, R., Hall, R. and Langsley, G. ( 1998). Upregulation of Jun and Fos family members and permanent JNK activity lead to constitutive AP-1 activation in Theileria-transformed leukocytes. Molecular and Biochemical Parasitology 94, 215226.CrossRefGoogle Scholar
Dessauge, F., Hilaly, S., Baumgartner, M., Blumen, B., Werling, D. and Langsley, G. ( 2005 a). c-Myc activation by Theileria parasites promotes survival of infected B-lymphocytes. Oncogene 24, 10751083.Google Scholar
Dessauge, F., Lizundia, R., Baumgartner, M., Chaussepied, M. and Langsley, G. ( 2005 b). Taking the Myc is bad for Theileria. Trends in Parasitology 21, 377385.Google Scholar
Dessauge, F., Lizundia, R. and Langsley, G. ( 2005 c). Constitutively activated CK2 potentially plays a pivotal role in Theileria-induced lymphocyte transformation. Parasitology 130, S37S44.Google Scholar
Dhand, R., Hiles, I., Panayotou, G., Roche, S., Fry, M. J., Gout, I., Totty, N. F., Truong, O., Vicendo, P., Yonezawa, K., Kasuga, M., Courteneidge, S. A. and Waterfield, M. D. ( 1994). PI 3-kinases is a dual specificity enzyme: autoregulation by an intrinsic protein-serine kinase activity. EMBO Journal 13, 522533.Google Scholar
Dobbelaere, D. A. and Kuenzi, P. ( 2004). The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Current Opinion in Immunology 16, 524530.CrossRefGoogle Scholar
Dobbelaere, D. A., Roditi, I. J., Coquerelle, T. M., Kelke, C., Eichhorn, M. and Williams, R. O. ( 1991). Lymphocytes infected with Theileria parva require both cell-cell contact and growth factor to proliferate. European Journal in Immunology 21, 8995.CrossRefGoogle Scholar
Dorin, D., Semblat, J. P., Poullet, P., Alano, P., Goldring, J. P., Whittle, C., Patterson, S., Chakrabarti, D. and Doerig, C. D. ( 2005). PfPK7, an atypical MEK-related protein kinase, reflects the absence of classical three-component MAPK pathways in the human malaria parasite Plasmodium falciparum. Molecular Microbiology 55, 184196.CrossRefGoogle Scholar
Fischer, S. F., Vier, J., Kirschnek, S., Klos, A., Hess, S., Ying, S. and Hacker, G. ( 2004). Chlamydia inhibit host cell apoptosis by degradation of proapoptotic BH3-only proteins. Journal of Experimental Medicine 200, 905916.CrossRefGoogle Scholar
Frevert, U., Galinski, M. R., Hugel, F. U., Allon, N., Schreier, H., Smulevitch, S., Shakibaei, M. and Clavijo, P. ( 1998). Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. EMBO Journal 17, 38163826.CrossRefGoogle Scholar
Galley, Y., Hagens, G., Glaser, I., Davis, W., Eichhorn, M. and Dobbelaere, D. ( 1997). Jun NH2-terminal kinase is constitutively activated in T cells transformed by the intracellular parasite Theileria parva. Proceedings of the National Academy of Sciences, USA 94, 51195124.CrossRefGoogle Scholar
Guergnon, J., Chaussepied, M., Sopp, P., Lizundia, R., Moreau, M. F., Blumen, B., Werling, D., Howard, C. J. and Langsley, G. ( 2003 a). A tumour necrosis factor alpha autocrine loop contributes to proliferation and nuclear factor-kappaB activation of Theileria parva-transformed B cells. Cellular Microbiology 5, 709716.Google Scholar
Guergnon, J., Dessauge, F., Langsley, G. and Garcia, A. ( 2003 b). Apoptosis of Theileria-infected lymphocytes induced upon parasite death involves activation of caspases 9 and 3. Biochimie 85, 771776.Google Scholar
Guergnon, J., Dessauge, F., Traincard, F., Cayla, X., Rebollo, A., Bost, E., Langsley, G. and Garcia, A. ( 2006). A PKA survival pathway inhibited by DPT-PKI, a new specific cell permeable PKA inhibitor, is induced by T. annulata in parasitized B-lymphocytes. Apoptosis, [Epub ahead of print].Google Scholar
Hafalla, J. C., Morrot, A., Sano, G., Milon, G., Lafaille, J. J. and Zavala, F. ( 2003). Early self-regulatory mechanisms control the magnitude of CD8+ T cell responses against liver stages of murine malaria. Journal of Immunology 171, 964970.CrossRefGoogle Scholar
Heussler, V. T., Fernandez, P. C., Machado, J. Jr., Botteron, C. and Dobbelaere, D. A. ( 1999 a). N-acetylcysteine blocks apoptosis induced by N-alpha-tosyl-L-phenylalanine chloromethyl ketone in transformed T-cells. Cell Death and Differentiation 6, 342350.Google Scholar
Heussler, V. T., Kuenzi, P., Fraga, F., Schwab, R. A., Hemmings, B. A. and Dobbelaere, D. A. ( 2001). The Akt/PKB pathway is constitutively activated in Theileria-transformed leucocytes, but does not directly control constitutive NF-kappaB activation. Cellular Microbiology 3, 537550.CrossRefGoogle Scholar
Heussler, V. T., Machado, J. Jr., Fernandez, P. C., Botteron, C., Chen, C. G., Pearse, M. J. and Dobbelaere, D. A. ( 1999 b). The intracellular parasite Theileria parva protects infected T cells from apoptosis. Proceedings of the National Academy of Sciences, USA 96, 73127317.Google Scholar
Heussler, V. T., Rottenberg, S., Schwab, R., Kuenzi, P., Fernandez, P. C., McKellar, S., Shiels, B., Chen, Z. J., Orth, K., Wallach, D. and Dobbelaere, D. A. ( 2002). Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 298, 10331036.CrossRefGoogle Scholar
Huber, S. M., Duranton, C., Henke, G., Van de Sand, C., Heussler, V., Shumilina, E., Sandu, C. D., Tanneur, V., Brand, V., Kasinathan, R. S., Lang, K. S., Kremsner, P. G., Hubner, C. A., Rust, M. B., Dedek, K., Jentsch, T. J. and Lang, F. ( 2004). Plasmodium induces swelling-activated ClC-2 anion channels in the host erythrocyte. Journal of Biological Chemistry 279, 4144441452.CrossRefGoogle Scholar
Ivanov, V., Stein, B., Baumann, I., Dobbelaere, D. A., Herrlich, P. and Williams, R. O. ( 1989). Infection with the intracellular protozoan parasite Theileria parva induces constitutively high levels of NF-kappa B in bovine T lymphocytes. Molecular and Cellular Biology 9, 46774686.CrossRefGoogle Scholar
Johnson, D. E. ( 2000). Noncaspase proteases in apoptosis. Leukemia 14, 16951703.CrossRefGoogle Scholar
Kamata, H., Honda, S., Maeda, S., Chang, L., Hirata, H. and Karin, M. ( 2005). Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120, 649661.CrossRefGoogle Scholar
Kuenzi, 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, 12241231.CrossRefGoogle Scholar
Kumar, A., Takada, Y., Boriek, A. M. and Aggarwal, B. B. ( 2004). Nuclear factor-kappaB: its role in health and disease. Journal of Molecular Medicine 82, 434448.Google Scholar
Lane, H. A., Fernandez, A., Lamb, N. J. C. and Thomas, G. ( 1993). p70s6k function is essential for G1 progression. Nature 363, 170172.CrossRefGoogle Scholar
Lang, F., Lang, P. A., Lang, K. S., Brand, V., Tanneur, V., Duranton, C., Wieder, T. and Huber, S. M. ( 2004). Channel-induced apoptosis of infected host cells-the case of malaria. Pflugers Archive: European Journal of Physiology 448, 319324.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 a). HGF/MET signalling protects Plasmodium-infected host cells from apoptosis. Cellular Microbiology 7, 603609.Google Scholar
Leiriao, P., Mota, M. M. and Rodriguez, A. ( 2005 b). Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells. Journal of Infectious Diseases 191, 15761581.Google Scholar
Lizundia, R., Chaussepied, M., Huerre, M., Werling, D., Di santo, J. P. and Langsley, G. ( 2006). JNK/cJun signalling promotes survival and metastasis of B-lymphocytes transformed by Theileria. Cancer Research 66, 61056110.CrossRefGoogle Scholar
Lizundia, R., Sengmanivong, L., Guergnon, J., Muller, 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, 629635.CrossRefGoogle Scholar
Luder, C. G., Lang, C., Giraldo-Velasquez, M., Algner, M., Gerdes, J. and Gross, U. ( 2003). Toxoplasma gondii inhibits MHC class II expression in neural antigen-presenting cells by down-regulating the class II transactivator CIITA. Journal of Neuroimmunology 134, 1224.CrossRefGoogle Scholar
Luder, C. G., Walter, W., Beuerle, B., Maeurer, M. J. and Gross, U. ( 2001). Toxoplasma gondii down-regulates MHC class II gene expression and antigen presentation by murine macrophages via interference with nuclear translocation of STAT1alpha. European Journal of Immunology 31, 14751484.3.0.CO;2-C>CrossRefGoogle Scholar
Meis, J. F., Verhave, J. P., Jap, P. H. and Meuwissen, J. H. ( 1985). Fine structure of exoerythrocytic merozoite formation of Plasmodium berghei in rat liver. Journal of Protozoology 32, 694699.CrossRefGoogle Scholar
Ocana-Morgner, C., Mota, M. M. and Rodriguez, A. ( 2003). Malaria blood stage suppression of liver stage immunity by dendritic cells. Journal of Experimental Medicine 197, 143151.CrossRefGoogle Scholar
O'Shea, C. C. ( 2005). Viruses – seeking and destroying the tumor program. Oncogene 24, 76407655.CrossRefGoogle Scholar
Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C. A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Coulson, R. M., Cronin, A., De villiers, E. P., Fraser, A., Fosker, N., Gardner, M., Goble, A., Griffiths-Jones, S., Harris, D. E., Katzer, F., Larke, N., Lord, A., Maser, P., McKellar, S., Mooney, P., Morton, F., Nene, V., O'Neil, S., Price, C., Quail, M. A., Rabbinowitsch, E., Rawlings, N. D., Rutter, S., Saunders, D., Seeger, K., Shah, T., Squares, R., Squares, S., Tivey, A., Walker, A. R., Woodward, J., Dobbelaere, D. A., Langsley, G., Rajandream, M. A., McKeever, D., Shiels, B., Tait, A., Barrell, B. and Hall, N. ( 2005). Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 309, 131133.CrossRefGoogle Scholar
Palmer, G. H., Machado, J. Jr., Fernandez, P., Heussler, V., Perinat, T. and Dobbelaere, D. A. ( 1997). Parasite-mediated nuclear factor kappaB regulation in lymphoproliferation caused by Theileria parva infection. Proceedings of the National Academy of Sciences, USA 94, 1252712532.CrossRefGoogle Scholar
Pelengaris, S., Khan, M. and Evan, G. ( 2002). c-MYC: more than just a matter of life and death. Nature Reviews-Cancer 2, 764776.CrossRefGoogle Scholar
Shapira, S., Harb, O. S., Caamano, J. and Hunter, C. A. ( 2004). The NF-kappaB signaling pathway: immune evasion and immunoregulation during toxoplasmosis. International Journal for Parasitology 34, 393400.CrossRefGoogle Scholar
Shiels, B., Langsley, G., Weir, W., Pain, A., McKellar, S. and Dobbelaere, D. ( 2005). Alteration of host cell phenotype by Theileria annulata and Theileria parva: mining for manipulators in the parasite genomes. International Journal for Parasitology 36, 921.Google Scholar
Shiels, B. R., McKellar, S., Katzer, F., Lyons, K., Kinnaird, J., Ward, C., Wastling, J. M. and Swan, D. ( 2004). A Theileria annulata DNA binding protein localized to the host cell nucleus alters the phenotype of a bovine macrophage cell line. Eukaryotic Cell 3, 495505.CrossRefGoogle Scholar
Sobolewski, P., Gramaglia, I., Frangos, J. A., Intaglietta, M. and Van der heyde, H. ( 2005). Plasmodium berghei resists killing by reactive oxygen species. Infection and Immunity 73, 67046710.CrossRefGoogle Scholar
Stokoe, D., Stephens, L. R., Copeland, T., Gaffney, P. R. J., Reese, C. B., Painter, G. F., Holmes, A. B., McCormick, F. and Hawkins, P. T. ( 1997). Dual role of phosphatidylinositol-3,4,5-triphosphate in the activation of protein kinase B. Science 277, 567570.CrossRefGoogle Scholar
Terzakis, J. A., Vanderberg, J. P., Foley, D. and Shustak, S. ( 1979). Exoerythrocytic merozoites of Plasmodium berghei in rat hepatic Kupffer cells. Journal of Protozoology 26, 385389.CrossRefGoogle Scholar
van de Sand, C., Horstmann, S., Schmidt, A., Sturm, A., Bolte, S., Krueger, A., Lutgehetmann, M., Pollok, J. M., Libert, C. and Heussler, V. T. ( 2005). The liver stage of Plasmodium berghei inhibits host cell apoptosis. Molecular Microbiology 58, 731742.CrossRefGoogle Scholar
Weston, C. R. and Davis, R. J. ( 2002). The JNK signal transduction pathway. Current Opinion in Genetics and Development 12, 1421.CrossRefGoogle Scholar
Wickham, M. E., Culvenor, J. G. and Cowman, A. F. ( 2003). Selective inhibition of a two-step egress of malaria parasites from the host erythrocyte. Journal of Biological Chemistry 278, 3765837663.CrossRefGoogle Scholar