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Programmed cell death in a human intestinal parasite, Blastocystis hominis

Published online by Cambridge University Press:  28 November 2001

A. M. A. NASIRUDEEN ,
K. S. W. TAN ,
M. SINGH  and
E. H. YAP
A. M. A. NASIRUDEEN
Affiliation:
Department of Microbiology, Faculty of Medicine, National University of Singapore, 5 Science Drive 2, Singapore 117597
K. S. W. TAN
Affiliation:
Department of Microbiology, Faculty of Medicine, National University of Singapore, 5 Science Drive 2, Singapore 117597
M. SINGH
Affiliation:
Department of Microbiology, Faculty of Medicine, National University of Singapore, 5 Science Drive 2, Singapore 117597
E. H. YAP
Affiliation:
Department of Microbiology, Faculty of Medicine, National University of Singapore, 5 Science Drive 2, Singapore 117597
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Abstract

Although programmed cell death (PCD) has been associated with multicellular organisms, there have been more reports of its presence in some protozoans. Our study shows the existence of PCD in an intestinal protozoan, Blastocystis hominis. Light and electron microscopy, biochemical and flow cytometry studies showed apoptosis-like death in B. hominis cells exposed to a cytotoxic monoclonal antibody (MAb 1D5). B. hominis cells displayed key morphological and biochemical features of apoptosis, namely, nuclear condensation and in situ fragmentation, reduced cytoplasmic volume, some externalization of phosphatidylserine and maintenance of plasma membrane integrity. No oligonucleosomal DNA laddering was observed in gel electrophoresis. This study supports earlier observations that the cellular machinery that is required to carry out PCD may have existed before the advent of multicellularity. Our study also ascribes a novel function for the B. hominis central vacuole in apoptosis; it acts as a repository where apoptotic bodies are stored before being released into the extracellular space.

Keywords

apoptosisprogrammed cell deathBlastocystisprotozoamonoclonal antibody
Type
Research Article
Information
Parasitology , Volume 123 , Issue 3 , March 2001 , pp. 235 - 246
Copyright
© 2002 Cambridge University Press

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References

AMEISEN, J. C., IDZIOREK, T., BILLANT-MULOT, O., LOYENS, M., TISSNER, J., POTENTIER, A. & OMAISSI, 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
BARBIERI, D., TROIANO, L., GRASSILLI, E., AGNESINI, C., CRISTOFALO, E. A., MONTI, D., CAPRI, M., COSSARIZZA, A. & FRANCESCHI, C. (1992). Inhibition of apoptosis by zinc: a reappraisal. Biochemistry and Biophysics Research Communication 187, 1256–1261.CrossRefGoogle Scholar
COHEN, G. M., SUN, X., SNOWDEN, R. T., DINSDALE, D. & SKILLETER, D. N. (1992). Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochemistry Journal 286, 331–334.CrossRefGoogle Scholar
COLLINS, R. J., HARMON, B. V., GOBE, G. C. & KERR, J. F. R. (1992). Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. International Journal of Radiation Biology 61, 451–453.CrossRefGoogle Scholar
COLLINS, J. A., SCHANDL, C. A., YOUNG, K. K., VESELY, J. & WILLINGHAM, M. C. (1997). Major DNA fragmentation is a late event in apoptosis. Journal of Histochemistry and Cytochemistry 45, 923–934.CrossRefGoogle Scholar
CORNILLON, S., FOA, C., DAVOUST, J., BUONAVISTA, N., GROSS, J. D. & GOLSTEIN, P. (1994). Programmed cell death in Dictyostelium. Journal of Cell Science 107, 2691–2704.Google Scholar
DARZYNKIEWICZ, Z., JUAN, G., LI, X., GORCZYCA, W., MURAKAMI, T. & TRAGANOS, F. (1997). Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27, 1–20.3.0.CO;2-L>CrossRefGoogle Scholar
DUNN, L. A., BOREHAM, P. F. L. & STENZEL, D. J. (1989). Ultrastructural variation of Blastocystis hominis stocks in culture. International Journal for Parasitology 19, 43–56.CrossRefGoogle Scholar
ELLIS, R. E., YUAN, J. & HORVITZ, H. R. (1991). Mechanisms and functions of cell death. Annual Reviews of Cell Biology 7, 663–698.CrossRefGoogle Scholar
FALCIERI, E., MARTELLI, A. M., BAREGGI, R., CATALDI, A. & COCCO, L. (1993). The protein kinase inhibitor staurosporine induces morphological changes typical of apoptosis in Molt-4 cells without concomitant DNA fragmentation. Biochemistry and Biophysics Research Communication 193, 19–25.CrossRefGoogle Scholar
FERLINI, C., KUNKL, A., SCAMBIA, G. & FATTOROSSI, A. (1997). The use of Apostain in identifying early apoptosis. Journal of Immunological Methods 205, 95–101.CrossRefGoogle Scholar
GATTI, R., BELLETTI, S., ORLANDINI, G., BUSSOLATI, O., DALL'ASTA, V. & GAZZOLA, G. C. (1998). Comparison of Annexin V and Calcein-AM as early vital markers of apoptosis in adherent cells by confocal laser microscopy. Journal of Histochemistry and Cytochemistry 46, 895–900.CrossRefGoogle Scholar
HIRATA, H., HIBASAMI, H., YOSHIDA, T., MORITA, A., OHKAYA, S., MATSUMOTO, M., SASAKI, H. & UCHIDA, A. (1998). Differentiation and apoptosis without DNA fragmentation in cultured Schwann cells derived from wallerian-degenerated nerve. Apoptosis 3, 353–360.CrossRefGoogle Scholar
HO, L. C., SINGH, M., SURESH, G., NG, G. C. & YAP, E. H. (1993). Axenic culture of Blastocystis hominis in Iscove's modified Dulbecco's medium. Parasitology Research 79, 614–616.CrossRefGoogle Scholar
HOWELL, D. M. & MARTZ, E. (1987). The degree of CTL-induced DNA solubilization is not determined by the human vs mouse origin of the target cell. Journal of Immunology 138, 3695–3698.Google Scholar
KERR, J. F. R., SEARLE, J., HARMON, B. V. & BISHOP, C. J. (1987). Apoptosis. In Perspectives on Mammalian Cell Death (ed. POTTEN, C. S.), pp. 93–128. Oxford University Press, Oxford.
KERR, J. F. R., WYLLIE, A. H. & 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
MESNER, P. W., WINTERS, T. R. & GREEN, S. H. (1992). Nerve growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. Journal of Cell Biology 199, 1669–1680.CrossRefGoogle Scholar
MOE, K. T., SINGH, M., HOWE, J., HO, L. C., TAN, S. W., CHEN, X. Q. & YAP, E. H. (1999). Development of Blastocystis hominis cysts into vacuolar forms in vitro. Parasitology Research 85, 103–108.CrossRefGoogle Scholar
MOREIRA, M. E. L., PORTILLO, H. A. D., MILDER, R. V., BALANCO, J. M. F. & 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. & 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
PAKANDL, M. (1999). Blastocystis sp. from pigs: ultrastructural changes occurring during polyxenic cultivation in Iscove's modified Dulbecco's medium. Parasitology Research 85, 743–748.Google Scholar
PENFOLD, P. L. & PROVIS, J. M. (1986). Cell death in the development of the human retina: phagocytosis of pyknotic and apoptotic bodies by retinal cells. Graefe's Archive for Clinical and Experimental Opthalmology 224, 549–553.CrossRefGoogle Scholar
PICOT, S., BURNOD, J., BRACCHI, V., CHUMPITAZI, B. F. F. & 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, London 356, 397–400.CrossRefGoogle Scholar
RIDGLEY, E. L., XIONG, Z. & RUBEN, L. (1999). Reactive oxygen species activate a Ca2+-dependent cell death pathway in the unicellular organism Trypanosoma brucei. Biochemistry Journal 340, 33–40.CrossRefGoogle Scholar
STELLER, H. (1995). Mechanisms and genes of cellular suicide. Science 267, 1445–1449.CrossRefGoogle Scholar
STENZEL, D. J. & BOREHAM, P. F. L. (1996). Blastocystis hominis revisited. Clinical Microbiology Review 9, 563–584.Google Scholar
STENZEL, D. J., DUNN, L. A. & BOREHAM, P. F. L. (1989). Endocytosis in cultures of Blastocystis hominis. International Journal for Parasitology 19, 787–791.CrossRefGoogle Scholar
TAN, S. W., HO, L. C., MOE, K. T., CHEN, X. Q., NG, G. C., YAP, E. H. & SINGH, M. (1996). Production and characterization of murine monoclonal antibodies to Blastocystis hominis. International Journal for Parasitology 26, 375–381.CrossRefGoogle Scholar
TAN, S. W., SINGH, M., HO, L. C., HOWE, J., MOE, K. T., CHEN, X. Q., NG, G. C. & YAP, E. H. (1997). Survival of Blastocystis hominis clones after exposure to a cytotoxic monoclonal antibody. International Journal for Parasitology 27, 947–954.CrossRefGoogle Scholar
UCKER, D. S., OBERMILLER, P. S. & ECKHART, W. (1992). Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Molecular and Cell Biology 12, 3060–3069.CrossRefGoogle Scholar
VAUX, D. L. (1993). Towards an understanding of the molecular mechanisms of physiological cell death. Proceedings of the National Academy of Sciences, USA 90, 786–789.CrossRefGoogle Scholar
VAUX, D. L. & STRASSER, A. (1996). The molecular biology of apoptosis. Proceedings of the National Academy of Sciences, USA 93, 2239–2244.CrossRefGoogle Scholar
VERMES, I., HAANEN, C., STEFFENS-NAKKEN, H. & REUTELINGSPERGER, C. (1995). A novel assay for apoptosis: Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. Journal of Immunological Methods 184, 39–51.CrossRefGoogle Scholar
WELBURN, S. C., DALE, C., ELLIS, D., BEECROFT, R. & PEARSON, T. W. (1996). Apoptosis in procyclic Trypanosoma brucei rhodesiense in vitro. Cell Death and Differentiation 3, 229–236.Google Scholar
WELBURN, S. C., BARCINSKI, M. A. & WILLIAMS, G. T. (1997). Programmed cell death in trypanosomatids. Parasitology Today 13, 22–26.CrossRefGoogle Scholar
WILLINGHAM, M. C. (1999). Cytochemical method for the detection of apoptosis. Journal of Histochemistry and Cytochemistry 47, 1101–1109.CrossRefGoogle Scholar
WYLLIE, A. H. (1992). Apoptosis and the regulation of cell numbers in normal and neoplastic tissues: an overview. Cancer Metastasis Review 11, 93–103.CrossRefGoogle Scholar
YOSHIKAWA, H. & HAYAKAWA, A. (1996). Morphological changes in the central vacuole of Blastocystis hominis during in vitro culture. Protoplasm 194, 63–68.CrossRefGoogle Scholar