Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-22T18:53:05.579Z Has data issue: false hasContentIssue false
  • English
  • Français

Programmed cell death in African trypanosomes

Published online by Cambridge University Press:  03 October 2006

S. C. WELBURN ,
E. MACLEOD ,
K. FIGARELLA  and
M. DUZENSKO
S. C. WELBURN
Affiliation:
Centre for Infectious Diseases, College of Medicine and Veterinary Medicine, University of Edinburgh, EH25 9RG
E. MACLEOD
Affiliation:
Centre for Infectious Diseases, College of Medicine and Veterinary Medicine, University of Edinburgh, EH25 9RG
K. FIGARELLA
Affiliation:
Department of Biochemistry, University of Tubingen, Hoppe-Seyler-Str. 4, 72076 Tubingen, Germany
M. DUZENSKO
Affiliation:
Department of Biochemistry, University of Tubingen, Hoppe-Seyler-Str. 4, 72076 Tubingen, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

Until recently it had generally been assumed that apoptosis and other forms of programmed cell death evolved during evolution of the metazoans to regulate growth and development in these multicellular organisms. However, recent research is adding strength to the original phenotypic observations described almost a decade ago which indicated that some parasitic protozoa may have evolved a cell death pathway analogous to the process described as apoptosis in metazoa. Here we explore the implications of a programmed cell death pathway in the African tsetse-transmitted trypanosomes.

Keywords

Apoptosisprogrammed cell deathTrypanosoma bruceitrypanosomatids
Type
Research Article
Information
Parasitology , Volume 132 , Supplement S1: Programmed cell death and the protozoan parasite , March 2006 , pp. S7 - S18
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

Abello, P. A., Fidlerm, S. A. and Buchman, T. G. ( 1994). Thiol reducing agents modulate induced apoptosis in porcine endothelial cells. Shock 2, 79–83.CrossRefGoogle Scholar
Ahmed, A. M. and Hurd, H. ( 2006). Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes and Infection 8, 308–315.CrossRefGoogle Scholar
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, 1133–1143.CrossRefGoogle Scholar
Ameisen, J. C. ( 2002). On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death and Differentiation 9, 367–393.CrossRefGoogle Scholar
Ameisen, J. C., Idziorek, T., Billaut-Mulot, O., Loyens, M., Tissier, J. P., Potentier, A. and Ouaissi, A. ( 1995). Apoptosis in a unicellular eukaryote (Trypanosoma cruzi) – implications for the evolutionary origin and role of programmed cell death in the control of cell proliferation, differentiation and survival. Cell Death and Differentiation 2, 285–300.Google Scholar
Andreka, P., Tran, T., Webster, K. A. and Bishopric, N. H. ( 2004). Nitric oxide and promotion of cardiac myocyte apoptosis. Molecular and Cellular Biochemistry 263, 35–53.CrossRefGoogle Scholar
Ascenzi, P. and Gradoni, L. ( 2002). Nitric oxide limits parasite development in vectors and in invertebrate intermediate hosts. IUBMB Life 53, 121–123.Google Scholar
Ascenzi, P., Salvati, L., Bolognesi, M., Colasanti, M., Polticelli, F. and Venturini, G. ( 2001). Inhibition of cysteine protease activity by NO-donors. Current Protein Peptide Science 2, 137–153.CrossRefGoogle Scholar
Barcinski, M. A. and Moreira, M. E. C. ( 1994). Cellular response of protozoan parasites to host derived cytokines. Parasitology Today 10, 352–355.CrossRefGoogle Scholar
Barcinski, M. A., Schechtman, D., Quintao, L. G., Costa de A., Soares, L. R., Moreira, M. E. and Charlab, R. ( 1992). Granulocyte-macrophage colony stimulating factor increases the infectivity of Leishmania amazonensis by protecting promastigotes from heat induced cell death. Infection and Immunity 60, 3523–3527.Google Scholar
Bialik, S. and Kimchi, A. ( 2006). The death-associated protein kinases: structure, function, and beyond. Annual Review of Biochemistry 75, 189–210.CrossRefGoogle Scholar
Billaut-Mulot, O., Fernandez-Gomez, R., Loyens, M. and Ouaissi, A. ( 1996). Trypanosoma cruzi elongation factor 1-alpha: nuclear localization in parasites undergoing apoptosis. Gene 174, 19–26.Google Scholar
Black, S. J., Jack, R. M. and Marrison, W. I. ( 1983). Host-parasite interactions which influence the virulence of Trypanosoma (Trypanozoon) brucei brucei organisms. Acta Tropica 40, 11–18.Google Scholar
Breidbach, T., Ngazoa, E. and Steverding, D. ( 2002). Trypanosoma brucei: in vitro slender-to-stumpy differentiation of culture-adapted, monomorphic bloodstream forms. Experimental Parasitology 101, 223–230.CrossRefGoogle Scholar
Broker, L. E., Kruyt, F. A. and Giaccone, G. ( 2005). Cell death independent of caspases: a review. Clinical Cancer Research 11, 3155–3162.CrossRefGoogle Scholar
Caffrey, C. R., Hansell, E., Lucas, K. D., Brinen, L. S., Alvarez Hernandez, A., Cheng, J., Gwaltney, S. L., Roush, W. R., Stierhof, Y. D., Bogyo, M., Steverding, D. and McKerrow, J. H. ( 2001). Active site mapping, biochemical properties and subcellular localization of rhodesain, the major cysteine protease of Trypanosoma brucei rhodesiense. Molecular and Biochemical Parasitology 118, 61–73.CrossRefGoogle Scholar
Charlab, R., Blaineau, C., Schechtman, D. and Barcinski, M. A. ( 1990). Granulocyte-macrophage colony stimulating factor is a growth factor for promastigotes of Leishmania mexicana amazonensis. Journal of Protozoology 37, 352–357.CrossRefGoogle Scholar
Chaudhuri, M., Ajayi, W. and Hill, G. C. ( 1998). Biochemical and molecular properties of the Trypanosoma brucei alternative oxidase. Molecular and Biochemical Parasitology 95, 53–68.CrossRefGoogle Scholar
Chong, Z. Z., Li, F. and Maiese, K. ( 2005). Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Progress in Neurobiology 75, 207–246.CrossRefGoogle Scholar
Christensen, S. T., Chemnitz, J., Straarup, E. M., Kristiansen, K., Wheatley, D. N. and Rasmussen, L. ( 1998). Staurosporine-induced cell death in Tetrahymena thermophila has mixed characteristics of both apoptotic and autophagic degeneration. Cell Biology International 22, 591–598.Google Scholar
Christensen, S. T., Sorensen, H., Beyer, N. H., Kristiansen, K., Rasmussen, L. and Rasmussen, M. I. ( 2001). Cell death in Tetrahymena thermophila: new observations on culture conditions. Cell Biology International 25, 509–519.CrossRefGoogle Scholar
Christensen, S. T., Wheatley, D. N., Rasmussen, M. I. and Rasmussen, L. ( 1995). Mechanisms controlling death, survival and proliferation in a model unicellular eukaryote Tetrahymena thermophila. Cell Death and Differentiation 2, 301–308.Google Scholar
Clarke, A. R., Purdie, C. A., Harrison, D. J., Morris, R. G., Bird, C. C., Hooper, M. L. and Wyllie, A. H. ( 1993). Thymocyte apoptosis induced by P53-dependent and independent pathways. Nature 362, 849–852.CrossRefGoogle Scholar
Cornillon, S., Foa, C., Davoust, J., Buonavista, N., Gross, J. D. and Golstein, P. ( 1994). Programmed cell death in Dictyostelium. Journal of Cell Science 107, 2691–2704.Google Scholar
Cross, G. A. M. ( 1996). Antigenic variation in trypanosomes: Secrets surface slowly. BioEssays 18, 283–291.CrossRefGoogle Scholar
Curtin, J. F., Donovan, M. and Cotter, T. G. ( 2002). Regulation and measurement of oxidative stress in apoptosis. Journal of Immunological Methods 265, 49–72.CrossRefGoogle Scholar
Davis, M. C., Ward, J. G., Herrick, G. and Allis, C. D. ( 1992). Programmed nuclear death – apoptotic-like degredation of specific nuclei in conjugating Tetrahymena. Developmental Biology 154, 419–432.CrossRefGoogle Scholar
Deponte, M. and Becker, K. ( 2004). Plasmodium falciparum – do killers commit suicide? Trends in Parasitology 20, 165–169.Google Scholar
de Souza, E. M., Araujo-Jorge, T. C., Bailly, C., Lansiaux, A., Batista, M. M., Oliveira, G. M. and Soeiro, M. N. ( 2003). Host and parasite apoptosis following Trypanosoma cruzi infection in in vitro and in vivo models. Cell Tissue Research 314, 223–235.CrossRefGoogle Scholar
DosReis, G. A., Fonseca, M. E. F. and Lopes, M. F. ( 1995). Programmed T-cell death in experimental Chagas disease. Parasitology Today 11, 390–394.CrossRefGoogle Scholar
Ellis, R. E., Yuan, J. and Horvitz, H. R. ( 1991). Mechanisms and functions of cell-death. Annual Review of Cell Biology 7, 663–698.CrossRefGoogle Scholar
Engel, R. H. and Evens, A. M. ( 2006). Oxidative stress and apoptosis: a new treatment paradigm in cancer. Frontiers in Bioscience 11, 300–312.CrossRefGoogle Scholar
Evan, G. ( 1994). Old cells never die, they just apoptose. Trends in Cell Biology 4, 191–192.CrossRefGoogle Scholar
Fadeel, B. and Orrenius, S. ( 2005). Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. Journal of Internal Medicine 258, 479–517.CrossRefGoogle Scholar
Fairlamb, A. H., Blackburn, P., Ulrich, P., Chait, B. T. and Cerami, A. ( 1985). Trypanothione: a novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science 227, 1485–1487.CrossRefGoogle Scholar
Fang, J. and Beattie, D. S. ( 2003). Alternative oxidase present in procyclic Trypanosoma brucei may act to lower the mitochondrial production of superoxide. Archives of Biochemistry and Biophysics 414, 294–302.CrossRefGoogle Scholar
Figarella, K. ( 2005). PhD Thesis, Univerity of Tubingen, Germany.
Figarella, K., Rawer, M., Uzcategui, N. L., Kubata, B. K., Lauber, K., Madeo, F., Wesselborg, S. and Duszenko, M. ( 2005). Prostaglandin D2 induces programmed cell death in Trypanosoma brucei bloodstream form. Cell Death and Differentiation 12, 335–346.CrossRefGoogle Scholar
Figarella, K., Uzcategui, N. L., Beck, A., Schoenfeld, C., Kubata, B. K., Lang, F. and Duszenko, M. ( 2006). Prostaglandin-induced programmed cell death in Trypanosoma brucei involves oxidative stress. Cell Death and Differentiation (Epub ahead of print).CrossRefGoogle Scholar
Frohlich, K. U. and Madeo, F. ( 2000). Apoptosis in yeast – a monocellular organism exhibits altruistic behaviour. FEBS Letters 473, 6–9.CrossRefGoogle Scholar
Gugssa, A., Gebru, S., Lee, C. M., Baccetti, B. and Anderson, W. ( 2005). Apoptosis of Trypanosoma musculi co-cultured with LPS activated macrophages: enhanced expression of nitric oxide synthase INF-gamma and caspase. Journal of Submicroscopic Cytology and Pathology 37, 99–107.Google Scholar
Hammarton, T., Lillico, S., Welburn, S. C. and Mottram, J. C. ( 2005). Trypanosoma brucei MOB1 is required for accurate and efficient cytokinesis but not for exit from mitosis. Molecular Microbiology 56, 104–116.CrossRefGoogle Scholar
Hao, Z., Kasumba, I. and Aksoy, S. ( 2003). Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochemistry Molecular Biology 33, 1155–1164.CrossRefGoogle Scholar
Hesse, F., Selzer, P. M., Muhlstadt, K. and Duszenko, M. ( 1995). A novel cultivation technique for long term maintenance of bloodstream from trypanosomes in vitro. Molecular and Biochemical Parasitology 70, 157–166.CrossRefGoogle Scholar
Heussler, V. T., Kuenzi, P. and Rottenberg, S. ( 2001). Inhibition of apoptosis by intracellular protozoan parasites. International Journal for Parasitology 31, 1166–1176.CrossRefGoogle Scholar
Hochman, A. ( 1997). Programmed cell death in prokaryotes. Critical Reviews in Microbiology 23, 207–214.CrossRefGoogle Scholar
Holzmuller, P., Sereno, D., Cavaleyra, M., Mangot, I., Daulouede, S., Vincendeau, P. and Lemesre, J. L. ( 2002). Nitric oxide-mediated proteasome-dependent oligonucleosomal DNA fragmentation in Leishmania amazonensis amastigotes. Infection and Immunity 70, 3727–3735.CrossRefGoogle Scholar
Hurd, H. and Carter, V. ( 2004). The role of programmed cell death in Plasmodium-mosquito interactions. International Journal for Parasitology 34, 1459–1472.CrossRefGoogle Scholar
Kaiser, D. ( 1986). Control of multicellular development: Dictyostelium and Myxococcus. Annual Review of Genetics 20, 539–566.CrossRefGoogle Scholar
Kerr, J. F., Wyllie, A. H. and Currie, A. R. ( 1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer 26, 239–257.CrossRefGoogle Scholar
Khelef, N., Zychlinski, A. and Guiso, N. ( 1993). Bordetella pertussis induces apoptosis in macrophages – role of adenylate cyclase haemolysin. Infection and Immunity 61, 4064–4071.Google Scholar
Kim, R., Emi, M. and Tanabe, K. ( 2005). Caspase-dependent and -independent cell death pathways after DNA damage. Oncology Reports 14, 595–599.CrossRefGoogle Scholar
Kobayashi, T. and Endoh, H. ( 2003). Caspase-like activity in programmed nuclear death during conjugation of Tetrahymena thermophila. Cell Death and Differentiation 10, 634–640.CrossRefGoogle Scholar
Kubata, B. K., Duszenko, M., Kabututu, Z., Rawer, M., Szallies, A., Fujimori, K., Inui, T., Nozaki, T., Yamashita, K., Horii, T., Urade, Y. and Hayaishi, O. ( 2000). Identification of a novel prostaglandin f(2alpha) synthase in Trypanosoma brucei. Journal of Experimental Medicine 192, 1327–1338.CrossRefGoogle Scholar
Laragione, T., Bonetto, V., Casoni, F., Massignan, T., Bianchi, G., Gianazza, E. and Ghezzi, P. ( 2003). Redox regulation of surface protein thiols: identification of integrin alpha-4 as a molecular target by using redox proteomics. Proceedings of the National Academy of Sciences, USA 100, 14737–14741.CrossRefGoogle Scholar
Laun, P., Pichova, A., Madeo, F., Fuchs, J., Ellinger, A., Kohlwein, S., Dawes, I., Frohlich, K. U. and Breitenbach, M. ( 2001). Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Molecular Microbiology 39, 1166–1173.CrossRefGoogle Scholar
Le Bras, M., Clement, M. V., Pervaiz, S. and Brenner, C. ( 2005). Reactive oxygen species and the mitochondrial signalling pathway of cell death. Histology and Histopathology 20, 205–219.Google Scholar
Lee, N., Bertholet, S., Debrabant, A., Muller, J., Duncan, R. and Nakhasi, H. L. ( 2002). Programmed cell death in the unicellular protozoan parasite Leishmania. Cell Death and Differentiation 9, 53–64.CrossRefGoogle Scholar
Lewis, K. ( 2000). Programmed death in bacteria. Microbiology and Molecular Biology Reviews 64, 503–514.CrossRefGoogle Scholar
Li, C. Q. and Wogan, G. N. ( 2005). Nitric oxide as a modulator of apoptosis. Cancer Letters 226, 1–15.CrossRefGoogle Scholar
Lillico, S. G., Mottram, J. C., Murphy, N. B. and Welburn, S. C. ( 2002). Characterisation of the QM gene of Trypanosoma brucei. FEMS Microbiology Letters 211, 123–128.CrossRefGoogle Scholar
Lockshin, R. A. and Williams, C. M. ( 1964). Programmed cell death. II Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. Journal of Insect Physiology 10, 643–649.Google Scholar
Lopes, M. F., da Veiga, V. F., Santos, A. R., Fonseca, M. E. 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
Luckhart, S., Vodovotz, Y., Cui, L. and Rosenberg, R. ( 1998). The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Sciences, USA 95, 5700–5705.CrossRefGoogle Scholar
Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T., Barrientos, A. and Corte-Real, M. ( 2002). Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Molecular Biology of the Cell 13, 2598–2606.CrossRefGoogle Scholar
Ludovico, P., Sousa, M. J., Silva, M. T., Leao, C. and Corte-Real, M. ( 2001). Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147, 2409–2415.CrossRefGoogle Scholar
MacLeod, E. T. ( 2005). PhD Thesis, University of Edinburgh.
Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H. and Frohlich, K. U. ( 1999). Oxygen stress: a regulator of apoptosis in yeast. Journal of Cell Biology 145, 757–767.CrossRefGoogle Scholar
Mariante, R. M., Guimaraes, C. A., Linden, R. and Benchimol, M. ( 2003). Hydrogen peroxide induces caspase activation and programmed cell death in the amitochondrial Tritrichomonas foetus. Histochemistry and Cell Biology 120, 129–141.Google Scholar
Martz, E. and Howell, D. M. ( 1989). CTL: Virus controls cells first and cytolytic cells second? Immunology Today 10, 79–86.Google Scholar
Moore, K. J. and Matlashewski, G. ( 1994). Intracellular infection by Leishmania donovani inhibits macrophage apoptosis. Journal of Immunology 152, 2930–2937.Google Scholar
Moreira, M. E., Del Portillo, H. A., Milder, R. V., Balanco, J. M. and Barcinski, M. A. ( 1996). Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis. Journal of Cellular Physiology 167, 305–313.3.0.CO;2-6>CrossRefGoogle Scholar
Murphy, N. B. and Welburn, S. C. ( 1997). Programmed cell death in procyclic Trypanosoma brucei rhodesiense is associated with differential expression of mRNAs. Cell Death and Differentiation 4, 365–370.CrossRefGoogle Scholar
Nasirudeen, A. M., Singh, M., Yap, E. H. and Tan, K. S. ( 2001). Blastocystis hominis: Evidence for Caspase-3-like activity in cells undergoing programmed cell death. Parasitology Research 87, 559–565.Google Scholar
Naoi, M., Maruyama, W., Shamoto-Nagai, M., Yi, H., Akao, Y. and Tanaka, M. ( 2005). Oxidative stress in mitochondria: decision to survival and death of neurons in neurodegenerative disorders. Molecular Neurobiology 31, 81–93.CrossRefGoogle Scholar
Okoth, J. O. and Kapaata, R. ( 1986). Trypanosome infection rates in Glossina fuscipes fuscipes Newst. in the Busoga sleeping sickness focus, Uganda. Annals of Tropical Medicine and Parasitology 80, 459–461.CrossRefGoogle Scholar
Pearson, T., Beecroft, R., Welburn, S. C., Ruepp, S., Roditi, I., Hwa, K. Y., Englund, P. T., Wells, C. W. and Murphy, N. B. ( 2000). The major cell surface glycoprotein procyclin is a receptor for induction of a novel form of cell death in African trypanosomes in vitro. Molecular and Biochemical Parasitology 111, 333–349.CrossRefGoogle Scholar
Placenza, L., Peluffo, G. and Radi, R. ( 2001). L-arginine-dependent suppression of apoptosis in Trypanosoma cruzi: contribution of the nitric oxide and polyamine pathways. Proceedings of the National Academy of Sciences, USA 98, 7301–7306.CrossRefGoogle Scholar
Picot, S., Burnod, J., Bracchi, V., Chumpitazi, B. F. and Ambroise-Thomas, P. ( 1997). Apoptosis related to chloroquine sensitivity of the human malaria parasite Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 590–591.CrossRefGoogle Scholar
Raff, M. C. ( 1992). Social controls on cell-survival and cell-death. Nature 356, 397–400.CrossRefGoogle Scholar
Rice, K. C. and Bayles, K. W. ( 2003). Death's toolbox: examining the molecular components of bacterial programmed cell death. Molecular Microbiology 50, 729–738.CrossRefGoogle Scholar
Ridgley, E. L., Xiong, Z. H. and Ruben, L. ( 1999). Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei brucei. Biochemical Journal 340, 33–40.CrossRefGoogle Scholar
Rodrigues, M. M., Mendonça-Previato, L., Charlab, R. and Barcinski, M. A. ( 1987). The cellular immune response to a purified antigen from Leishmania mexicana subsp. amazonensis enhances the size of the leishmanial lesion on susceptible mice. Infection and Immunity 55, 3142–3148.Google Scholar
Rodrigues, M. M., Xavier, M. T., Previato, L. M. and Barcinski, M. A. ( 1986). Characterization of cellular immune response to chemically defined glycoconjugates from Leishmania mexicana subsp. amazonensis. Infection and Immunity 51, 80–86.Google Scholar
Ross, R. and Thompson, D. ( 1910). A case of sleeping sickness studied by precise enumerative methods: regular periodical increase of the parasites disclosed. Proceedings of the Royal Society of London, Series B 82, 411–415.CrossRefGoogle Scholar
Scory, S., Caffrey, C. R., Stierhof, Y. D., Ruppel, A. and Steverding, D. ( 1999). Trypanosoma brucei: killing of bloodstream forms in vitro and in vivo by the cysteine proteinase inhibitor Z-phe-ala-CHN2. Experimental Parasitology 91, 327–333.CrossRefGoogle Scholar
Seed, J. R. and Wenck, M. A. ( 2003). Role of the long slender to short stumpy transition in the life cycle of the African trypanosomes. Kinetoplastid Biology and Disease 2, 3.CrossRefGoogle Scholar
Sen, N., Das, B. B., Ganguly, A., Mukherjee, T., Bandyopadhyay, S. and Majunder, H. K. ( 2004). Camptothecin-induced imbalance in intracellular cation homeostasis regulates programmed cell death in unicellular hemoflagellate Leishmania donovani. Journal of Biological Chemistry 279, 52366–52375.CrossRefGoogle Scholar
Shen, Y. and Shenk, T. E. ( 1995). Viruses and apoptosis. Current Opinions in Genetics and Development 5, 105–111.CrossRefGoogle Scholar
Soares, L. R. and Barcinski, M. A. ( 1992). Differential production of granulocyte-macrophage colony-stimulating factor by macrophages from mice susceptible and resistant to Leishmania mexicana amazonensis. Journal of Leukocyte Biology 51, 220–224.CrossRefGoogle Scholar
Souza, A. V., Petretski, J. H., Demasi, M., Bechara, E. J. and Oliveira, P. L. ( 1997). Urate protects a blood-sucking insect against hemin-induced oxidative stress. Free Radical Biology and Medicine 22, 209–214.CrossRefGoogle Scholar
Szallies, A., Kubata, B. K. and Duszenko, M. ( 2002). A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS Letters 517, 144–150.CrossRefGoogle Scholar
Tan, K. S. and Nasirudeen, A. M. ( 2005). Protozoan programmed cell death – insights from Blastocystis deathstyles. Trends in Parasitology 21, 547–550.CrossRefGoogle Scholar
Tibayrenc, M., Kjellberg, F., Arnaud, J., Oury, B., Breniere, S. F., Darde, M. L. and Ayala, F. J. ( 1991). Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proceedings of the National Academy of Sciences, USA 88, 5129–5133.CrossRefGoogle Scholar
Troeberg, L., Morty, R. E., Pike, R. N., Lonsdale-Eccles, J. D., Palmer, J. T., McKerrow, J. H. and Coetzer, T. H. ( 1999). Cysteine proteinase inhibitors kill cultured bloodstream forms of Trypanosoma brucei brucei. Experimental Parasitology 91, 349–355.CrossRefGoogle Scholar
Tsuda, A., Witola, W. H., Ohashi, K. and Onuma, M. ( 2005). Expression of alternative oxidase inhibits programmed cell death-like phenomenon in bloodstream form of Trypanosoma brucei rhodesiense. Parasitology International 54, 243–251.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, 731–742.CrossRefGoogle Scholar
Vardi, A., Berman-Frank, I., Rozenberg, T., Hadas, O., Kaplan, A. and Levine, A. ( 1999). Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Current Biology 9, 1061–1064.CrossRefGoogle Scholar
Vassella, E., Reuner, B., Yutzy, B. and Boshart, M. ( 1997). Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. Journal of Cell Science 110, 2661–2671.Google Scholar
Vaux, D. L., Haecker, G. and Strasser, A. ( 1994). An evolutionary perspective on apoptosis. Cell 76, 777–779.CrossRefGoogle Scholar
Watanabe, N. and Lam, E. ( 2005). Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. Journal of Biological Chemistry 280 14691–14699.Google Scholar
Wanderley, J. L., Moreira, M. E., Benjamin, A., Bonomo, A. C. and Barcinski, M. A. ( 2006). Mimicry of apoptotic cells by exposing phosphatidylserine participates in the establishment of amastigotes of Leishmania (L.) amazonensis in mammalian hosts. Journal of Immunology 176, 1834–1839.Google Scholar
Welburn, S. C., Dale, C., Ellis, D., Beecroft, R. and Pearson, T. W. ( 1996). Apoptosis in procyclic Trypanosoma brucei rhodesiense in vitro. Cell Death and Differentiation 3, 229–236.Google Scholar
Welburn, S. C., Lillico, S. and Murphy, N. B. ( 1999). Programmed cell death in procyclic form Trypanosoma brucei rhodesiense – identification of differentially expressed genes during con A induced death. Memórias do Instituto Oswaldo Cruz 94, 229–234.CrossRefGoogle Scholar
Welburn, S. C. and Maudlin, I. ( 1997). Control of Trypanosoma brucei brucei infections in tsetse, Glossina morsitans. Medical and Veterinary Entomology 111, 286–289.CrossRefGoogle Scholar
Welburn, S. C., Maudlin, I. and Ellis, D. S. ( 1989). Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Medical and Veterinary Entomology 3, 77–82.CrossRefGoogle Scholar
Welburn, S. C., Maudlin, I. and Milligan, P. J. ( 1995). Trypanozoon: infectivity to humans is linked to reduced transmissibility in tsetse. I. Comparison of human serum-resistant and human serum-sensitive field isolates. Experimental Parasitology 81, 404–408.CrossRefGoogle Scholar
Welburn, S. C. and Murphy, N. B. ( 1998). Prohibitin and RACK homologues are up-regulated in trypanosomes induced to undergo apoptosis and in naturally occurring terminally differentiated forms. Cell Death and Differentiation 5, 615–622.CrossRefGoogle Scholar
White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steller, H. ( 1994). Genetic control of programmed cell-death in Drosophila. Science 264, 677–683.CrossRefGoogle Scholar
Williams, G. T. ( 1994). Apoptosis in the immune system. Journal of Pathology 173, 1–4.CrossRefGoogle Scholar
Wyllie, A. H. ( 1980). Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555–556.CrossRefGoogle Scholar
Wyllie, A. H., Kerr, J. F. R. and Curry, A. R. ( 1980). Cell death: the significance of apoptosis. International Review of Cytology 68, 251–306.CrossRefGoogle Scholar
Wyllie, A. H., Morris, R. G., Smith, A. L. and Dunlop, D. ( 1984). Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. Journal of Pathology 142, 67–77.CrossRefGoogle Scholar
Zangger, H., Mottram, J. C. and Fasel, N. ( 2002). Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? Cell Death and Differentiation 9, 1126–1139.Google Scholar
Zychlinsky, A., Prevost, M. C. and Sansonetti, P. J. ( 1992). Shigella flexneri induces apoptosis in infected macrophages. Nature 358, 167–169.CrossRefGoogle Scholar