Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T05:37:10.599Z Has data issue: false hasContentIssue false
  • English
  • Français

The malaria merozoite, forty years on

Published online by Cambridge University Press:  03 August 2009

L. H. BANNISTER  and
G. H. MITCHELL
L. H. BANNISTER*
Affiliation:
Centre for Ultrastructural Imaging, Guy's Campus, King's College London, London SE1 1UL, UK
G. H. MITCHELL
Affiliation:
Malaria Laboratory, Department of Immunobiology, Guy's, King's College and St Thomas' Hospitals' School of Medicine, KCL, Borough Wing, Guy's Hospital, Great Maze Pond, London SE1 9RT, UK
*
*Corresponding author: Centre for Ultrastructural Imaging, Guy's Campus, King's College London, London SE1 1UL, UK. Tel: +44(0)2086533042. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The invasive blood stage of malaria parasites, merozoites, are complex entities specialized for the capture and entry of red blood cells. Their potential for vaccination and other anti-malaria strategies have attracted much research attention over the last 40 years, and there is now a considerable body of data relating to their biology. In this article some of the major advances over this period and remaining challenges are reviewed.

Keywords

Plasmodiummalariamerozoitevaccinationmicroscopycell biologyinvasionhistory
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1435 - 1444
Copyright
Copyright © Cambridge University Press 2009

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

Adams, J. H., Hudson, D. E., Torii, M., Ward, G. E., Wellems, T. E., Aikawa, M. and Miller, L. H. (1990). The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 63, 141–153.CrossRefGoogle ScholarPubMed
Aikawa, M. (1967). Ultrastructure of the pellicular complex of Plasmodium fallax. Journal of Cell Biology 35, 103–113.CrossRefGoogle ScholarPubMed
Aikawa, M. (1971). Plasmodium: The fine structure of malarial parasites. Experimental Parasitology 30, 284–320.CrossRefGoogle ScholarPubMed
Aikawa, M., David, P., Fine, E., Hudson, D., Klotz, F. and Miller, L. H. (1986). Localization of protective 143/140 kDa antigens of Plasmodium knowlesi by the use of antibodies and ultracryomicrotomy. European Journal of Cell Biology 41, 207–213.Google ScholarPubMed
Aikawa, M., Miller, L. H., Johnson, J. and Rabbege, J. (1978). Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. Journal of Cell Biology 77, 77–82.Google ScholarPubMed
Aikawa, M., Miller, L. H., Rabbege, J. R. and Epstein, N. (1981). Freeze-fracture study on the erythrocyte membrane during malarial parasite invasion. Journal of Cell Biology 91, 55–62.CrossRefGoogle Scholar
Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Miller, J. A., Nayak, V., Pennington, C., Pinney, D. F., Roos, D. S., Ross, C., Stoeckert, C. J. Jr., Treatman, C. and Wang, H. (2009). PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Research 37, D539–D543.CrossRefGoogle ScholarPubMed
Baker, R. P., Wijetilaka, R. and Urban, S. (2006). Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria. PLoS Pathogens 2, 0922–0932.CrossRefGoogle ScholarPubMed
Bannister, L. H., Butcher, G. A., Dennis, E. D. and Mitchell, G. H. (1975). Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro. Parasitology 71, 483–491.CrossRefGoogle ScholarPubMed
Bannister, L. H. and Dluzewski, A. R. (1990). The ultrastructure of red cell invasion in malaria infections: a review. Blood Cells 16, 257–292.Google ScholarPubMed
Bannister, L. H., Hopkins, J. M., Dluzewski, A. R., Margos, G., Williams, I. T., Blackman, M. J., Kocken, C. H., Thomas, A. W. and Mitchell, G. H. (2003). 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 ScholarPubMed
Bannister, L. H., Mitchell, G. H., Butcher, G. A. and Dennis, E. D. (1986 a). Lamellar membranes associated with rhoptries in erythrocytic merozoites of Plasmodium knowlesi: a clue to the mechanism of invasion. Parasitology 92, 291–303.CrossRefGoogle Scholar
Bannister, L. H., Mitchell, G. H., Butcher, G. A., Dennis, E. D. and Cohen, S. (1986 b). Structure and development of the surface coat of erythrocytic merozoites of Plasmodium knowlesi. Cell and Tissue Research 245, 281–290.CrossRefGoogle ScholarPubMed
Baum, J., Richard, D., Healer, J., Rug, M., Krnajski, Z., Gilberger, T. W., Green, J. L., Holder, A. A. and Cowman, A. F. (2006). A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. Journal of Biological Chemistry 281, 5197–5208.CrossRefGoogle ScholarPubMed
Baum, J., Chen, L., Healer, J., Lopaticki, S., Boyle, M., Triglia, T., Ehlgen, F., Ralph, S. A., Beeson, J. G. and Cowman, A. F. (2009). Reticulocyte-binding protein homologue 5 – An essential adhesin involved in invasion of human erythrocytes by Plasmodium falciparum. International Journal for Parasitology 39, 371–380.CrossRefGoogle ScholarPubMed
Bejon, P. A., Bannister, L. H., Fowler, R. E., Fookes, R. E., Webb, S. E., Wright, A. and Mitchell, G. H. (1997). A role for microtubules in Plasmodium falciparum merozoite invasion. Parasitology 114, 1–6.CrossRefGoogle ScholarPubMed
Besteiro, S., Bertrand-Michel, J., Lebrun, M., Vial, H. and Dubremetz, J. F. (2008). Lipidomic analysis of Toxoplasma gondii tachyzoites rhoptries: further insights into the role of cholesterol. The Biochemical Journal 415, 87–96.CrossRefGoogle ScholarPubMed
Butcher, G. and Cohen, S. (1970). Schizogony of Plasmodium knowlesi in the presence of normal and immune sera. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 470.CrossRefGoogle ScholarPubMed
Butcher, G. A., Mitchell, G. H. and Cohen, S. (1973). Mechanism of host specificity in malarial infecton. Nature, London 244, 40–42.CrossRefGoogle Scholar
Camus, D. and Hadley, T. J. (1985). A Plasmodium falciparum antigen that binds to host erythrocytes and merozoites. Science 230, 553–556.CrossRefGoogle ScholarPubMed
Coggeshall, L. T. and Kumm, W. H. (1937). Demonstration of passive immunity in experimental monkey malaria. Journal of Experimental Medicine 66, 177–190.CrossRefGoogle ScholarPubMed
Cohen, S., McGregor, I. A. and Carrington, S. (1961). Gamma-globulin and acquired immunity to human malaria. Nature, London 192, 733–737.CrossRefGoogle ScholarPubMed
Cohen, S. and Butcher, G. A. (1971). Serum antibody in acquired malarial immunity. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 125–135.CrossRefGoogle ScholarPubMed
Cohen, S., Butcher, G. A., Mitchell, G. H., Deans, J. A. and Langhorne, J. (1977). Acquired immunity and vaccination in malaria. American Journal of Tropical Medicine and Hygiene 26, 223–232.CrossRefGoogle ScholarPubMed
Cowman, A. F. and Crabb, B. S. (2006). Invasion of red blood cells by malaria parasites. Cell 124, 755–766.CrossRefGoogle ScholarPubMed
Cyrklaff, M., Kudryashev, M., Leis, A., Leonard, K., Baumeister, W., Ménard, R., Meissner, M. and Frischknecht, F. (2007). Cryoelectron tomography reveals periodic material at the inner side of subpellicular microtubules in apicomplexan parasites. Journal of Experimental Medicine 204, 1281–1287.CrossRefGoogle ScholarPubMed
David, P. H., Hudson, D. E., Hadley, T. J., Klotz, F. W. and Miller, L. H. (1985). Immunization of monkeys with a 140 kilodalton merozoite surface protein of Plasmodium knowlesi malaria: appearance of alternate forms of this protein. The Journal of Immunology 134, 4146–4152.CrossRefGoogle ScholarPubMed
Deans, J. A. (1984). Protective antigens of bloodstage Plasmodium knowlesi parasites. Philosophical Transactions of the Royal Society of London, B 307, 159–169.Google ScholarPubMed
Deans, J. A., Alderson, T., Thomas, A. W., Mitchell, G. H., Lennox, E. S. and Cohen, S. (1982). Rat monoclonal antibodies which inhibit the in vitro multiplication of Plasmodium knowlesi. Clinical and Experimental Immunology 49, 297–309.Google ScholarPubMed
Deans, J. A., Knight, A. M., Jean, W. C., Waters, A. P., Cohen, S. and Mitchell, G. H. (1988). Vaccination trials in rhesus monkeys with a minor, invariant, Plasmodium knowlesi 66 kD merozoite antigen. Parasite Immunology 10, 535–552.CrossRefGoogle ScholarPubMed
Dluzewski, A. R., Rangachari, K., Wilson, R. J. and Gratzer, W. B. (1983). A cytoplasmic requirement of red cells for invasion by malarial parasites. Molecular and Biochemical Parasitology 9, 145–160.CrossRefGoogle ScholarPubMed
Dluzewski, A. R., Mitchell, G. H., Fryer, P. R., Griffiths, S., Wilson, R. J. and Gratzer, W. B. (1992). Origins of the parasitophorous vacuole membrane of the malaria parasite, Plasmodium falciparum, in human red blood cells. Journal of Cell Science 102, 527–532.CrossRefGoogle ScholarPubMed
Dluzewski, A. R., Zicha, D., Dunn, G. A. and Gratzer, W. B. (1995). Origins of the parasitophorous vacuole membrane of the malaria parasite: surface area of the parasitized red cell. European Journal of Cell Biology 68, 446–449.Google ScholarPubMed
Dowse, T. J., Koussis, K., Blackman, M. J. and Soldati-Favre, D. (2008). Roles of proteases during invasion and egress by Plasmodium and Toxoplasma. Sub-Cellular Biochemistry 47, 121–139.CrossRefGoogle ScholarPubMed
Dvorak, J. A., Miller, L. H., Whitehouse, W. C. and Shiroishi, T. (1975). Invasion of erythrocytes by malaria merozoites. Science 187, 748–750.CrossRefGoogle ScholarPubMed
Field, S. J., Rangachari, K., Dluzewski, A. R., Wilson, R. J. and Gratzer, W. B. (1992). Effect of intra-erythrocytic magnesium ions on invasion by Plasmodium falciparum. Parasitology 105, 15–19.CrossRefGoogle ScholarPubMed
Field, S. J., Pinder, J. C., Clough, B., Dluzewski, A. R., Wilson, R. J. and Gratzer, W. B. (1993). Actin in the merozoite of the malaria parasite, Plasmodium falciparum. Cell Motility and the Cytoskeleton 25, 43–48.CrossRefGoogle ScholarPubMed
Freeman, R. R. and Holder, A. A. (1983). Surface antigens of malaria merozoites. A high molecular weight precursor is processed to an 83,000 mol wt form expressed on the surface of Plasmodium falciparum merozoites. Journal of Experimental Medicine 158, 1647–1653.CrossRefGoogle Scholar
Galinski, M. R., Dluzewski, A. R. and Barnwell, J. W. (2005). A mechanistic approach to merozoite invasion of red blood cells. In Molecular Approaches to Malaria (ed. Sherwin, I. R.), pp. 1–61. ASM Press, Washington, USA.Google Scholar
Garnham, P. C. C., Bird, R. G. and Baker, J. R. (1960). Electron microscope studies of motile stages of malaria parasites. I. The fine structure of the sporozoites of Haemamoeba (Plasmodium) gallinacea. Transactions of the Royal Society of Tropical Medicine and Hygiene 54, 274–278.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Blackwells, Oxford, UK.Google Scholar
Gilson, P. R., Nebl, T., Vukcevic, D., Moritz, R. L., Sargeant, T., Speed, T. P., Schofield, L. and Crabb, B. S. (2006). Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Molecular and Cellular Proteomics 57, 1286–1299.CrossRefGoogle Scholar
Hadley, T., Aikawa, M. and Miller, L. H. (1983) Plasmodium knowlesi: studies on invasion of rhesus erythrocytes by merozoites in the presence of protease inhibitors. Experimental Parasitology 55, 306–311.CrossRefGoogle ScholarPubMed
Harris, P. K., Yeoh, S., Dluzewski, A. R., O'Donnell, R. A., Withers-Martinez, C., Hackett, F., Bannister, L. H., Mitchell, G. H. and Blackman, M. J. (2005). Molecular identification of a malaria merozoite surface sheddase. PLoS Pathogens 1, 241–251.CrossRefGoogle ScholarPubMed
Haynes, J. D., Diggs, C. L., Hines, F. A. and Desjardins, R. E. (1976). Culture of human malaria parasites Plasmodium falciparum. Nature, London 263, 767–769.CrossRefGoogle ScholarPubMed
Heidrich, H. G., Matzner, M., Miettinen-Baumann, A. and 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 ScholarPubMed
Heidrich, H. G., Strych, W. and Mrema, J. E. (1983). Identification of surface and internal antigens from spontaneously released Plasmodium falciparum merozoites by radio-iodination and metabolic labelling. Zeitschrift für Parasitenkunde 69, 715–725.CrossRefGoogle ScholarPubMed
Heintzelman, M. B. and Schwartzman, J. D. (1997). A novel class of unconventional myosins from Toxoplasma gondii. Journal of Molecular Biology 27, 139–146.CrossRefGoogle Scholar
Hepler, P. K., Huff, C. G. and Sprinz, H. (1966). The fine structure of the exo-erythrocytic stages of Plasmodium fallax. Journal of Cell Biology 30, 333–358.CrossRefGoogle Scholar
Holder, A. A. and Freeman, R. R. (1984). Protective antigens of rodent and human bloodstage malaria. Philosophical Transactions of the Royal Society of London, B 307, 171–177.Google ScholarPubMed
Jacobs, L. (1967). Toxoplasma and toxoplasmosis. Advances in Parasitology 5, 1–5.CrossRefGoogle ScholarPubMed
Ladda, R., Aikawa, M. and Sprinz, H. (1969). Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites. Journal of Parasitology 87, 470–478.Google Scholar
Langreth, S. G., Jensen, J. B., Reese, R. T. and Trager, W. (1978). Fine structure of human malaria in vitro. Journal of Protozoology 25, 443–452.CrossRefGoogle ScholarPubMed
Ling, I. T., Florens, L., Dluzewski, A. R., Kaneko, O., Grainger, M., Yim Lim, B. Y. S., Tsuboi, T., Hopkins, J. M., Johnson, J. R., Torii, M., Bannister, L. H., Yates, I. I. I. Jr., Holder, A. A. and Mattei, D. (2004). The Plasmodium falciparum clag9 gene encodes a rhoptry protein that is transferred to the host erythrocyte upon invasion. Molecular Microbiology 52, 107–118.CrossRefGoogle Scholar
Mason, S. J., Miller, L. H., Shiroshi, T., Dvorak, J. A. and McGinniss, M. H. (1977). The Duffy blood group determinants: Their role in the susceptibility of humans and animal erythrocytes to Plasmodium knowlesi malaria. British Journal of Haematology 36, 327–335.CrossRefGoogle ScholarPubMed
Matuschewski, K. and Mueller, A. K. (2007). Vaccines against malaria – an update. FEBS Journal 274, 4680–4687.CrossRefGoogle ScholarPubMed
McGhee, R. B. (1951). The adaptation of the avian malaria parasite Plasmodium lophurae to a continuous existence in baby mice. Journal of Infectious Diseases 88, 86–97.CrossRefGoogle Scholar
McLaren, D. J., Bannister, L. H., Trigg, P. I. and Butcher, G. A. (1979). Freeze fracture studies on the interaction between the malaria parasite and the host erythrocyte in Plasmodium knowlesi infections. Parasitology 79, 125–139.CrossRefGoogle ScholarPubMed
Miller, L. H., Aikawa, M., Johnson, J. G. and Shiroishi, T. (1979). Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. Journal of Experimental Medicine 149, 172–184.CrossRefGoogle ScholarPubMed
Miller, L. H., Mason, S. J., Dvorak, J. A., McGinniss, M. H. and Rothman, I. K. (1975). Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189, 561–563.CrossRefGoogle ScholarPubMed
Mitchell, G. H., Butcher, G. A., Voller, A. and Cohen, S. (1976). The effect of human immune IgG on the in vitro development of Plasmodium falciparum. Parasitology 72, 149–162.CrossRefGoogle ScholarPubMed
Mitchell, G. H., Hadley, T. J., McGinniss, M. H., Klotz, F. W. and Miller, L. H. (1986). Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood 67, 1519–1521.CrossRefGoogle ScholarPubMed
Mitchell, G. H., Thomas, A. W., Margos, G., Dluzewski, A. R. and Bannister, L. H. (2004). Apical membrane antigen 1, a major malaria vaccine candidate, mediates the close attachment of invasive merozoites to host red blood cells. Infection and Immunity 72, 154–158.CrossRefGoogle Scholar
Murphy, S. C., Fernandez-Pol, S., Chung, P. H., Prasanna Murthy, S. N., Milne, S. B., Salomao, M., Brown, H. A., Lomasney, J. W., Mohandas, N. and Haldar, K. (2007). Cytoplasmic remodeling of erythrocyte raft lipids during infection by the human malaria parasite Plasmodium falciparum. Blood 110, 2132–2139.CrossRefGoogle ScholarPubMed
Nussenzweig, R. S., Vanderberg, J., Spitalny, G. L., Rivera, C. I. O., Orton, C. and Most, H. (1972). Sporozoite-induced immunity in mammalian malaria: A review. American Journal of Tropical Medicine and Hygiene 21, 722–728.CrossRefGoogle ScholarPubMed
Oka, M., Aikawa, M. and Freeman, R. R. (1984). Ultrastructural localization of protective antigens of Plasmodium yoelii merozoites by the use of monoclonal antibodies and ultrathin cryomicrotomy. American Journal of Tropical Medicine and Hygiene 33, 342–346.CrossRefGoogle ScholarPubMed
Pain, A. and Hertz-Fowler, C. (2009). Plasmodium genomics: latest milestone. Nature Reviews Microbiology 7, 180–181.CrossRefGoogle ScholarPubMed
Pasvol, G. (2003). How many pathways for invasion of the red blood cell by the malaria parasite? Trends in Parasitology 19, 430–432.CrossRefGoogle ScholarPubMed
Pasvol, G. (2007). Eroding the resistance of Duffy negativity to invasion by Plasmodium vivax? Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 953–954.CrossRefGoogle ScholarPubMed
Pinder, J. C., Fowler, R. E., Dluzewski, A. R., Bannister, L. H., Lavin, F. M., Mitchell, G. H., Wilson, R. J. M. and Gratzer, W. B. (1998). Actomyosin motor in the merozoite of the malaria parasite, Plasmodium falciparum: implications for red cell invasion. Journal of Cell Science 111, 1831–1839.CrossRefGoogle ScholarPubMed
Remarque, E. J., Faber, B. W., Kocken, C. H. M. and Thomas, A. W. (2008). Apical membrane antigen 1: a malaria vaccine candidate in review. Trends in Parasitology 24, 74–84.CrossRefGoogle ScholarPubMed
Rudzinska, M. A. and Trager, W. (1959). Phagotrophy and two new structures in the malaria parasite Plasmodium berghei. Journal of Biophysical and Biochemical Cytology 6, 103–112.CrossRefGoogle ScholarPubMed
Russell, P. F. and Mohan, B. N. (1942). The immunization of fowls against mosquito-borne Plasmodium gallinaceum by injections of serum and inactivated homologous sporozoites. The Journal of Experimental Medicine 76, 477–495.CrossRefGoogle ScholarPubMed
Scholtyseck, E. and Mehlhorn, H. (1970). Ultrastructural study of characteristic organelles (paired organelles, micronemes, micropores) of sporozoa and related organisms. Zeitschrift für Parasitenkunde 34, 97–127.CrossRefGoogle ScholarPubMed
Schrével, J., Asfaux-Foucher, G., Hopkins, J. M., Robert, V., Bourgouin, C., Prensier, G. and Bannister, L. H. (2007). Vesicle trafficking during sporozoite development in Plasmodium berghei: ultrastructural evidence for a novel trafficking mechanism. Parasitology 135, 1–12.CrossRefGoogle ScholarPubMed
Sénaud, J. (1967). Contribution à l'étude des Sarcosporidies et des Toxoplasmes (Toxoplasmea). Protistologica 3, 167–232.Google Scholar
Thera, M. A., Doumbo, O. K., Coulibaly, D., Diallo, D. A., Kone, A. K., Guindo, A. B., Traore, K., Dicko, A., Sagara, I., Sissoko, M. S., Baby, M., Sissoko, M., Diarra, I., Niangaly, A., Dolo, A., Daou, M., Diawara, S. I., Heppner, D. G., Stewart, V. A., Angov, E., Bergmann-Leitner, E. S., Lanar, D. E., Dutta, S., Soisson, L., Diggs, C. L., Leach, A., Owusu, A., Dubois, M.-C., Cohen, J., Nixon, J. N., Gregson, A., Takala, S. L., Lyke, K. E. and Plowe, C. V. (2008). Safety and immunogenicity of an AMA-1 malaria vaccine in Malian adults: Results of a phase 1 randomized controlled trial. PLoS One 3, e1465.CrossRefGoogle ScholarPubMed
Thomas, A. W., Deans, J. A., Mitchell, G. H., Alderson, T. and Cohen, S. (1984). The Fab fragments of monoclonal IgG to a merozoite surface antigen inhibit Plasmodium knowlesi invasion of erythrocytes. Molecular and Biochemical Parasitology 13, 187–199.CrossRefGoogle ScholarPubMed
Trager, W. and Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–675.CrossRefGoogle ScholarPubMed
Treeck, M., Zacherl, S., Herrmann, S., Cabrera, A., Kono, M., Struck, N. S., Engelberg, K., Haase, S., Frischknecht, F., Miura, K., Spielmann, T. and Gilberger, T. W. (2009). Functional analysis of the leading malaria vaccine candidate AMA-1 reveals an essential role for the cytoplasmic domain in the invasion process. PLoS Pathogens 5, e10000322.CrossRefGoogle ScholarPubMed
van Dijk, M. R., Waters, A. P. and Janse, C. J. (1995). Stable transfection of malaria parasite blood stages. Science 268, 1358–1362.CrossRefGoogle ScholarPubMed
Ward, G. E., Miller, L. H. and Dvorak, J. A. (1993). The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. Journal of Cell Science 106, 237–248.CrossRefGoogle ScholarPubMed
Webb, S. E., Fowler, R. E., O'Shaughnessy, C., Pinder, J. C., Dluzewski, A. R., Gratzer, W. B., Bannister, L. H. and Mitchell, G. H. (1996). Contractile protein system in the asexual stages of the malaria parasite Plasmodium falciparum. Parasitology 112, 451–457.CrossRefGoogle ScholarPubMed
Wu, Y., Kirkman, L. A. and Wellems, T. E. (1996). Transformation of Plasmodium falciparum malaria parasites by homologous integration of plasmids that confer resistance to pyrimethamine. Proceedings of the National Academy of Sciences, USA 93, 1130–1134.CrossRefGoogle ScholarPubMed
Yeoh, S., O'Donnell, R. A., Koussis, K., Dluzewski, A. R., Ansell, K. H., Osborne, S. A., Hackett, F., Withers-Martinez, C., Mitchell, G. H., Bannister, L. H., Bryans, J. S., Kettleborough, C. A. and Blackman, M. J. (2007). Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131, 1072–1083.CrossRefGoogle ScholarPubMed