Hostname: page-component-7dd5485656-frp75 Total loading time: 0 Render date: 2025-11-02T14:44:15.785Z Has data issue: false hasContentIssue false
  • English
  • Français

Correlation of structural development and differential expression of invasion-related molecules in schizonts of Plasmodium falciparum

Published online by Cambridge University Press:  23 August 2004

G. MARGOS ,
L. H. BANNISTER ,
A. R. DLUZEWSKI ,
J. HOPKINS ,
I. T. WILLIAMS  and
G. H. MITCHELL
G. MARGOS
Affiliation:
Department of Immunobiology, Guy's, Kings, and St Thomas' Schools of Medicine, Guy's Hospital, London SE1 9RT, UK
L. H. BANNISTER
Affiliation:
Department of Anatomy, Cell and Human Biology, GKT, School of Biomedical Sciences, London SE1 1UL, UK
A. R. DLUZEWSKI
Affiliation:
Department of Immunobiology, Guy's, Kings, and St Thomas' Schools of Medicine, Guy's Hospital, London SE1 9RT, UK
J. HOPKINS
Affiliation:
Department of Anatomy, Cell and Human Biology, GKT, School of Biomedical Sciences, London SE1 1UL, UK
I. T. WILLIAMS
Affiliation:
Department of Immunobiology, Guy's, Kings, and St Thomas' Schools of Medicine, Guy's Hospital, London SE1 9RT, UK
G. H. MITCHELL
Affiliation:
Department of Immunobiology, Guy's, Kings, and St Thomas' Schools of Medicine, Guy's Hospital, London SE1 9RT, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

During asexual development Plasmodium schizonts undergo a series of complex biochemical and structural changes. Using tightly synchronized cultures of 2 P. falciparum lines (clone C10 and strain ITO4) for light microscopy and fluorescence imaging we monitored the timing and sequence of expression of proteins associated with invasion-related organelles. Antibodies to rhoptry, micronemal and dense granule proteins (Rhoptry Associated Protein 1, Apical Membrane Antigen 1, Erythrocyte Binding Antigen 175, Ring-infected Erythrocyte Surface Antigen) and to pellicle-associated proteins (Merozoite Surface Protein 1, PfMyosin-A) were used. Clone C10 developed faster than ITO4; this difference was also found in the timing of protein expression seen by immunofluorescence. Light microscopic data were combined with transmission electron microscopic analysis using serial sectioning of ITO4 schizonts to determine nuclear number and organellar development. Thus a timetable of schizont structural maturation was established. Generally, the timing of organelle-specific antigen expression correlates well with the ultrastructural data. Rhoptries are formed mainly between second and fourth nuclear divisions, micronemes between the end of the fourth nuclear division and merozoite separation from the residual body, while dense granules are generated mainly after the micronemes. PfAMA-1 appears in micronemes before EBA-175, suggesting micronemal heterogeneity.

Keywords

Plasmodium falciparumschizontmerozoite developmentimmunolocalizationultrastructuretime-courseorganelles

Information

Type
Research Article
Information
Parasitology , Volume 129 , Issue 3 , September 2004 , pp. 273 - 287
Copyright
© 2004 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.)

Article purchase

Temporarily unavailable

References

REFERENCES

AIKAWA, M. ( 1966). The fine structure of the erythrocytic stages of three avian malarial parasites, Plasmodium fallax, P. lophurae, and P. cathemerium. American Journal of Tropical Medicine and Hygiene 15, 449–471.CrossRefGoogle Scholar
AIKAWA, M., HUFF, C. G. & SPRINZ, H. ( 1967). Fine structure of the asexual stages of Plasmodium elongatum. Journal of Cell Biology 34, 229–249.CrossRefGoogle Scholar
AIKAWA, M., TORII, M., SJOLANDER, A., BERZINS, K., PERLMANN, P. & MILLER, L. H. ( 1990). Pf155/RESA antigen is localized in dense granules of Plasmodium falciparum merozoites. Experimental Parasitology 71, 326–329.CrossRefGoogle Scholar
ANDERS, R. F., BARZAGA, N., SHI, P. T., SCANLON, D. B., BROWN, L. E., THOMAS, L. M., BROWN, G. V., STAHL, H. D., COPPEL, R. L. & KEMP, D. J. ( 1987). Repetitive sequences in malaria antigens. In Molecular Strategies of Parasitic Invasion (ed. Agabian, N., Goodman, H. & Noguiera, N.), pp. 333–342. Alan R. Liss, Inc, New York.
BANNISTER, L. H., HOPKINS, J. M., DLUZEWSKI, A. R., MARGOS, G., WILLIAMS, I. T., BLACKMAN, M. J., KOCKEN, C. H., THOMAS, A. W. & MITCHELL, G. H. ( 2003). The Plasmodium falciparum Apical Membrane Antigen-1 (PfAMA-1) is translocated within micronemes along subpellicular microtubules during merozoite development. Journal of Cell Science 116, 3825–3834.CrossRefGoogle Scholar
BANNISTER, L. H., HOPKINS, J. M., FOWLER, R. E., KRISHNA, S. & MITCHELL, G. H. ( 2000 a). A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitology Today 16, 427–433.Google Scholar
BANNISTER, L. H., HOPKINS, J. M., FOWLER, R. E., KRISHNA, S. A. & MITCHELL, G. H. ( 2000 b). Ultrastructure of rhoptry development in Plasmodium falciparum erythrocytic schizonts. Parasitology 121, 273–287.Google Scholar
BANNISTER, L. H., HOPKINS, J. M., MARGOS, G., DLUZEWSKI, A. R. & MITCHELL, G. H. ( 2004). Three-dimensional ultrastructure of the ring stage of Plasmodium falciparum: evidence for export pathways. Microscopy and Microanalysis (in the Press).CrossRefGoogle Scholar
BANNISTER, L. H. & MITCHELL, G. H. ( 1986). Lipidic vacuoles in Plasmodium knowlesi erythrocytic schizonts. Journal of Protozoology 33, 271–275.CrossRefGoogle Scholar
BANNISTER, L. H. & MITCHELL, G. H. ( 1995). The role of the cytoskeleton in Plasmodium falciparum merozoite biology: an electron-microscopic view. Annals of Tropical Medicine and Parasitology 89, 105–111.CrossRefGoogle Scholar
BERGMAN, L. W., KAISER, K., FUJIOKA, H., COPPENS, I., DALY, T. M., FOX, S., MATUSCHEWSKI, K., NUSSENZWEIG, V. & KAPPE, S. H. ( 2003). Myosin A tail domain interacting protein (MTIP) localizes to the inner membrane complex of Plasmodium sporozoites. Journal of Cell Science 116, 39–49.CrossRefGoogle Scholar
BLACKMAN, M. J. & BANNISTER, L. H. ( 2001). Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Molecular and Biochemical Parasitology 117, 11–25.CrossRefGoogle Scholar
BOYD, M. F. ( 1949). A photographic atlas of human Plasmodia. In Malariology (ed. Boyd, M. F.), pp. 122–144. Saunders, Philadelphia.
BOZDECH, Z., LLINAS, M., PULLIAM, B. L., WONG, E. D., ZHU, J. & DERISI, J. L. ( 2003). The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. Public Library of Science Biology 1, E5.CrossRefGoogle Scholar
BRACCHI-RICARD, V., BARIK, S., DELVECCHIO, C., DOERIG, C., CHAKRABARTI, R. & CHAKRABARTI, D. ( 2000). PfPK6, a novel cyclin-dependent kinase/mitogen-activated protein kinase-related protein kinase from Plasmodium falciparum. The Biochemical Journal 347, 255–263.CrossRefGoogle Scholar
BROWN, G. V., CULVENOR, J. G., CREWTHER, P. E., BIANCO, A. E., COPPEL, R. L., SAINT, R. B., STAHL, H. D., KEMP, D. J. & ANDERS, R. F. ( 1985). Localization of the ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum in merozoites and ring-infected erythrocytes. Journal of Experimental Medicine 162, 774–779.CrossRefGoogle Scholar
BRUCE-CHWATT, L. J., WARRELL, D. A. & GILLES, H. M. ( 1993). The malaria parasites. In Bruce-Chwatt's Essential Malariology (ed. Gilles, H. M. & Warrell, D. A.), pp. 10–34. Edward Arnold, London.
CARRUTHERS, V. B. ( 1999). Armed and dangerous: Toxoplasma gondii uses an arsenal of secretory proteins to infect host cells. Parasitology International 48, 1–10.Google Scholar
CRANMER, S. L., MAGOWAN, C., LIANG, J., COPPEL, R. L. & COOKE, B. M. ( 1997). An alternative to serum for cultivation of Plasmodium falciparum in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 363–365.CrossRefGoogle Scholar
DLUZEWSKI, A. R., LING, I. T., RANGACHARI, K., BATES, P. A. & WILSON, R. J. ( 1984). A simple method for isolating viable mature parasites of Plasmodium falciparum from cultures. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 622–624.CrossRefGoogle Scholar
DOOLITTLE, R. F. ( 2002). The grand assault. Nature, London 419, 493–494.CrossRefGoogle Scholar
DUBREMETZ, J. F., GARCIA-REGUET, N., CONSEIL, V. & FOURMAUX, M. N. ( 1998). Apical organelles and host-cell invasion by Apicomplexa. International Journal for Parasitology 28, 1007–1013.CrossRefGoogle Scholar
EL SHOURA, S. M. ( 1994). Falciparum malaria in naturally infected human patients: VIII. Fine structure of intraerythrocytic asexual forms before and during chloroquine treatment. Applied Parasitology 35, 207–218.Google Scholar
ETZION, Z., MURRAY, M. C. & PERKINS, M. E. ( 1991). Isolation and characterization of rhoptries of Plasmodium falciparum. Molecular and Biochemical Parasitology 47, 51–61.CrossRefGoogle Scholar
FLORENS, L., WASHBURN, M. P., RAINE, J. D., ANTHONY, R. M., GRAINGER, M., HAYNES, J. D., MOCH, J. K., MUSTER, N., SACCI, J. B., TABB, D. L., WITNEY, A. A., WOLTERS, D., WU, Y., GARDNER, M. J., HOLDER, A. A., SINDEN, R. E., YATES, J. R. & CARUCCI, D. J. ( 2002). A proteomic view of the Plasmodium falciparum life cycle. Nature, London 419, 520–526.CrossRefGoogle Scholar
FOWLER, R. E., SMITH, A. M. C., WHITEHORN, J., WILLIAMS, I. T., BANNISTER, L. H. & MITCHELL, G. H. ( 2001). Microtubule associated motor proteins of Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 117, 187–200.CrossRefGoogle Scholar
FREEMAN, R. R. & HOLDER, A. A. ( 1983). Light microscope morphology of Plasmodium falciparum during a synchronized growth cycle in vitro. Annals of Tropical Medicine and Parasitology 77, 95–96.CrossRefGoogle Scholar
GARNHAM, P. C. C. ( 1966). Malaria Parasites and other Haemosporidia. Blackwell Scientific Publications, Oxford.
HEALER, J., CRAWFORD, S., RALPH, S., McFADDEN, G. & COWMAN, A. F. ( 2002). Independent translocation of two micronemal proteins in developing Plasmodium falciparum merozoites. Infection and Immunity 70, 5751–5758.CrossRefGoogle Scholar
HEIDRICH, H. G., MATZNER, M., MIETTINEN-BAUMANN, A. & STRYCH, W. ( 1986). Immunoelectron microscopy shows that the 80,000-dalton antigen of Plasmodium falciparum merozoites is localized in the surface coat. Zeitschrift für Parasitenkunde 72, 681–683.CrossRefGoogle Scholar
HEMPELMANN, E., LING, I. & WILSON, R. J. ( 1981). S-antigens and isozymes in strains of Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 855–858.CrossRefGoogle Scholar
HOLDER, A. A., BLACKMAN, M. J., BURGHAUS, P. A., CHAPPEL, J. A., LING, I. T., McCALLUM-DEIGHTON, N. & SHAI, S. ( 1992). A malaria merozoite surface protein (MSP1)-structure, processing and function. Memorias do Instituto Oswaldo Cruz 87 (Suppl. 3), 37–42.CrossRefGoogle Scholar
HOPKINS, J., FOWLER, R., KRISHNA, S., WILSON, I., MITCHELL, G. & BANNISTER, L. ( 1999). The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protistology 150, 283–295.CrossRefGoogle Scholar
HOWELL, S. A., WITHERS-MARTINEZ, C., KOCKEN, C. H., THOMAS, A. W. & BLACKMAN, M. J. ( 2001). Proteolytic processing and primary structure of Plasmodium falciparum apical membrane antigen-1. Journal of Biological Chemistry 276, 31311–31320.CrossRefGoogle Scholar
INGRAM, L. T., STENZEL, D. J., KARA, U. A. & BUSHELL, G. R. ( 1988). Localisation of internal antigens of Plasmodium falciparum using monoclonal antibodies and colloidal gold. Parasitology Research 74, 208–215.CrossRefGoogle Scholar
JAIKARIA, N. S., ROZARIO, C., RIDLEY, R. G. & PERKINS, M. E. ( 1993). Biogenesis of rhoptry organelles in Plasmodium falciparum. Molecular and Biochemical Parasitology 57, 269–279.CrossRefGoogle Scholar
KOCKEN, C. H., WITHERS-MARTINEZ, C., DUBBELD, M. A., VAN DER, W. A., HACKETT, F., VALDERRAMA, A., BLACKMAN, M. J. & THOMAS, A. W. ( 2002). High-level expression of the malaria blood-stage vaccine candidate Plasmodium falciparum apical membrane antigen 1 and induction of antibodies that inhibit erythrocyte invasion. Infection and Immunity 70, 4471–4476.CrossRefGoogle Scholar
LADDA, R. L. ( 1969). New insights into the fine structure of rodent malarial parasites. Military Medicine 134, 825–865.CrossRefGoogle Scholar
LAMBROS, C. & VANDERBERG, J. P. ( 1979). Synchronization of Plasmodium falciparum intraerythrocytic stages in culture. Journal of Physiology 65, 418–420.Google Scholar
LANGRETH, S. G., JENSEN, J. B., REESE, R. T. & TRAGER, W. ( 1978). Fine structure of human malaria in vitro. Journal of Protozoology 25, 443–452.CrossRefGoogle Scholar
LASONDER, E., ISHIHAMA, Y., ANDERSEN, J. S., VERMUNT, A. M., PAIN, A., SAUERWEIN, R. W., ELING, W. M., HALL, N., WATERS, A. P., STUNNENBERG, H. G. & MANN, M. ( 2002). Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature, London 419, 537–542.CrossRefGoogle Scholar
LE ROCH, K. G., ZHOU, Y., BLAIR, P. L., GRAINGER, M., MOCH, J. K., HAYNES, J. D., DE, L. V HOLDER, A. A., BATALOV, S., CARUCCI, D. J. & WINZELER, E. A. ( 2003). Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301, 1503–1508.CrossRefGoogle Scholar
MIETTINEN-BAUMANN, A., STRYCH, W., McBRIDE, J. & HEIDRICH, H. G. ( 1988). A 46,000 dalton Plasmodium falciparum merozoite surface glycoprotein not related to the 185,000–195,000 dalton schizont precursor molecule: isolation and characterization. Parasitology Research 74, 317–323.CrossRefGoogle Scholar
NARUM, D. L. & THOMAS, A. W. ( 1994). Differential localization of full-length and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 67, 59–68.CrossRefGoogle Scholar
ORLANDI, P. A., SIM, B. K., CHULAY, J. D. & HAYNES, J. D. ( 1990). Characterization of the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum. Molecular and Biochemical Parasitology 40, 285–294.CrossRefGoogle Scholar
PERKINS, M. ( 1988). Stage-dependent processing and localization of a Plasmodium falciparum protein of 130,000 molecular weight. Experimental Parasitology 65, 61–68.CrossRefGoogle Scholar
PERLMANN, H., BERZINS, K., WAHLGREN, M., CARLSSON, J., BJORKMAN, A., PATARROYO, M. E. & PERLMANN, P. ( 1984). Antibodies in malarial sera to parasite antigens in the membrane of erythrocytes infected with early asexual stages of Plasmodium falciparum. Journal of Experimental Medicine 159, 1686–1704.CrossRefGoogle Scholar
PINDER, J. C., FOWLER, R. E., DLUZEWSKI, A. R., BANNISTER, L. H., LAVIN, F. M., MITCHELL, G. H., WILSON, R. J. M. & GRATZER, W. B. ( 1998). An actomyosin motor in the merozoite of the malaria parasite Plasmodium falciparum: implications for red cell invasion. Journal of Cell Science 111, 1831–1839.Google Scholar
READ, M., SHERWIN, T., HOLLOWAY, S. P., GULL, K. & HYDE, J. E. ( 1993). Microtubular organisation visualized by immunofluorescence microscopy during erythrocytic schizogony in Plasmodium falciparum and investigation of the post-translational modifications of parasite tubulin. Parasitology 106, 223–232.CrossRefGoogle Scholar
ROBERTS, D. J., CRAIG, A. G., BERENDT, A. R., PINCHES, R., NASH, G., MARSH, K. & NEWBOLD, C. I. ( 1992). Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature, London 357, 689–692.CrossRefGoogle Scholar
SALMON, B. L., OKSMAN, A. & GOLDBERG, D. E. ( 2001). Malaria parasite exit from the host erythrocyte: a two-step process requiring extraerythrocytic proteolysis. Proceedings of the National Academy of Sciences, USA 98, 271–276.CrossRefGoogle Scholar
SIM, B. K., TOYOSHIMA, T., HAYNES, J. D. & AIKAWA, M. ( 1992). Localization of the 175-kilodalton erythrocyte binding antigen in micronemes of Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 51, 157–159.CrossRefGoogle Scholar
TARASCHI, T. F., TRELKA, D., SCHNEIDER, T. & MATTHEWS, I. ( 1998). Plasmodium falciparum: characterization of organelle migration during merozoite morphogenesis in asexual malaria infections. Experimental Parasitology 88, 184–193.CrossRefGoogle Scholar
VICKERMAN, K. & COX, F. E. G. ( 1967). Merozoite formation in the erythrocytic stages of the malaria parasite Plasmodium vinckei. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 303–312.CrossRefGoogle Scholar
WEBB, S. E., FOWLER, R. E., O'SHAUGHNESSY, C., PINDER, J. C., DLUZEWSKI, A. R., GRATZER, W. B., BANNISTER, L. H. & MITCHELL, G. H. ( 1996). Contractile protein system in the asexual stages of the malaria parasite. Parasitology 112, 451–457.CrossRefGoogle Scholar
WICKHAM, M. E., CULVENOR, J. G. & COWMAN, A. F. ( 2003). Selective inhibition of a two-step egress of malaria parasites from the host erythrocyte. Journal of Biological Chemistry 278, 37658–37663.CrossRefGoogle Scholar
WINGER, L. A., TIRAWANCHAI, N., NICHOLAS, J., CARTER, H. E., SMITH, J. E. & SINDEN, R. E. ( 1988). Ookinete antigens of Plasmodium berghei. Appearance on the zygote surface of an Mr 21 kD determinant identified by transmission-blocking monoclonal antibodies. Parasite Immunology 10, 193–207.Google Scholar