Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-19T06:41:40.791Z Has data issue: false hasContentIssue false

Molecular mechanisms of sequestration in malaria

Published online by Cambridge University Press:  06 April 2009

A. R. Berendt
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
D. J. P. Ferguson
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
J. Gardner
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
G. Turner
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
A. Rowe
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
C. McCormick
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
D. Roberts
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
A. Craig
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
R. Pinches
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
B. C. Elford
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK
C. I. Newbold
Affiliation:
Molecular Parasitology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Headington, Oxford OX3 9DU, UK

Extract

Cell surface molecules have received intense attention in recent years because of the central roles they play at the interface between the external environment and the cellular interior. Their functions include adhesion to other cells or extracellular matrices, protection against hostile physical, chemical and biological agents and the transport of metabolites into and out of the cell. In addition, cell surface molecules transduce signals across the cell membrane, relaying information inwards and presenting altered characteristics to the exterior as the environment changes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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

Aikawa, M., Brown, A., Smith, C. D., Tegoshi, T., Howard, R. J., Hasler, T. H., Ito, Y., Perry, G., Collins, w. E. & Webster, K. (1992). A primate model for human cerebral malaria: Plasmodium coatneyi-infected rhesus monkeys. American Journal of Tropical Medicine and Hygiene 46, 391–7.CrossRefGoogle ScholarPubMed
Barnwell, J. W., Asch, A. S., Nachman, R. L., Yamaya, M., Aikawa, M. & Ingravallo, P. (1989). A human 88-kD membrane glycoprotein (CD36) functions in vitro as a receptor for a cytoadherence ligand on Plasmodium falciparum-infected erythrocytes. Journal of Clinical Investigation 84, 765–72.CrossRefGoogle ScholarPubMed
Barnwell, J. W., Howard, R. J., Coon, H. G. & Miller, L. H. (1983). Splenic requirement for antigenic variation and expression of the variant antigen on the erythrocyte membrane in cloned Plasmodium knowlesi malaria. Infection and Immunity 40, 985–94.CrossRefGoogle ScholarPubMed
Barnwell, J. W., Howard, R. J. & Miller, L. H. (1983). Influence of the spleen on the expression of surface antigens on parasitised erythrocytes. CIBA Foundation Symposium 94, 117–36.Google Scholar
Barnwell, J. W., Ockenhouse, C. F. & Knowles, D. M. (1985). Monoclonal antibody OKM5 inhibits the in vitro binding of Plasmodium falciparum-infecled erythrocytes to monocytes, endothelial, and C32 melanoma cells. Journal of Immunology 135, 3494–7.CrossRefGoogle ScholarPubMed
Berendt, A. R., Ferguson, D. J. P. & Newbold, C. I. (1990). Sequestration in Plasmodium falciparum malaria: sticky cells and sticky problems. Parasitology Today 6, 247–54.Google Scholar
Berendt, A. R., McDowall, A., Craig, A. G., Bates, P. A., Sternberg, M. J., Marsh, K., Newbold, C. I. & Hogg, N. (1992). The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1-binding site. Cell 68, 7181.CrossRefGoogle ScholarPubMed
Berendt, A. R., Simmons, D. L., Tansey, J., Newbold, C. I. & Marsh, K. (1989). Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature 341, 57–9.CrossRefGoogle ScholarPubMed
Bevilacqua, B., Stengelin, S., Gimbrone, M. A. & Seed, B. (1989). Endothelial Leukocyte Adhesion Molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 243, 1160–4.CrossRefGoogle ScholarPubMed
Biggs, B. A., Anders, R. F., Dillon, H. E., Davern, K. M., Martin, M., Petersen, C. & Brown, G. V. (1992). Adherence of infected erythrocytes to venular endothelium selects for antigenic variants of Plasmodium falciparum. Journal of Immunology 149, 2047–54.CrossRefGoogle ScholarPubMed
Biggs, B. A., Culvenor, J. G., Ng, J. S., Kemp, D. J. & Brown, G. V. (1989). Plasmodium falciparum: cytoadherence of a knobless clone. Experimental Parasitology 69, 189–97.Google Scholar
Biggs, B. A., Gooze, L., Wycherley, K., Wollish, W., Southwell, B., Leech, J. H. & Brown, G. V. (1991). Antigenic variation in Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 88, 9171–4.Google Scholar
Bignami, A. & Bastianeli, A. (1889). Observations of estivo-autumnal malaria. Riforma Medico 6, 1334–5.Google Scholar
Brown, K. N. & Brown, I. N. (1965). Immunity to malaria: antigenic variation in chronic infections of Plasmodium knowlesi. Nature 208, 1286–8.CrossRefGoogle ScholarPubMed
Carlson, J., Ekre, H. P., Helmby, H., Gysin, J., Greenwood, B. M. & Wahlgren, M. (1992). Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. American Journal of Tropical Medicine and Hygiene 46, 595602.Google Scholar
Carlson, J., Helmby, H., Hill, A. V., Brewster, D., Greenwood, B. M. & Wahlgren, M. (1990). Human cerebral malaria: association with erythrocyte resetting and lack of anti-rosetting antibodies. Lancet 336, 1457–60.CrossRefGoogle Scholar
Cooke, B. M., Berendt, A. R., Craig, A. G., Mcgregor, J., Newbold, c. I. & Nash, G. B. (1994). Rolling and stationary cytoadhesion of red cells parasitised by Plasmodium falciparum: separate roles for ICAM-1, CD36 and thrombospondin. British Journal of Haematology, in press.Google Scholar
Crandall, I., Collins, W. E., Gysin, J. & Sherman, I. W. (1993). Synthetic peptides based on motifs present in human band 3 protein inhibit cytoadherence/sequestration of the malaria parasite Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 90, 4703–7.CrossRefGoogle ScholarPubMed
Crandall, I. & Sherman, I. w. (1991). Plasmodium falciparum (human malaria)-induced modifications in human erythrocyte band 3 protein. Parasitology 102, 335–40.CrossRefGoogle ScholarPubMed
David, P. H., Handunnetti, S. M., Leech, J. H., Gamage, p. & Mendis, K. N. (1988). Resetting: a new cytoadherence property of malaria-infected erythrocytes. American Journal of Tropical Medicine and Hygiene 38, 289–97.CrossRefGoogle Scholar
David, P. H., Hommel, M., Miller, L. H., Udeinya, I. J. & Oligino, L. D. (1983). Parasite sequestration in Plasmodium falciparum malaria: spleen and antibody modulation of cytoadherence of infected erythrocytes. Proceedings of the National Academy of Sciences, USA 80, 5075–9.CrossRefGoogle ScholarPubMed
Elford, B. C., Haynes, J. D., Chulay, J. D. & Wilson, R. J. (1985). Selective stage-specific changes in the permeability to small hydrophilic solutes of human erythrocytes infected with Plasmodium falciparum. Molecular and Biochemical Parasitology 16, 4360.CrossRefGoogle ScholarPubMed
Forsyth, K. P., Philip, G., Smith, T., Kum, E., Southwell, B. & Brown, G. V. (1989). Diversity of antigens expressed on the surface of erythrocytes infected with mature Plasmodium falciparum parasites in Papua New Guinea. American Journal of Tropical Medicine and Hygiene 41, 259–65.Google Scholar
Gilks, C. F., Walliker, D. & Newbold, C. I. (1990). Relationships between sequestration, antigenic variation and chronic parasitism in Plasmodium chabaudi chabaudi – a rodent malaria model. Parasite Immunology 12, 4564.CrossRefGoogle ScholarPubMed
Handunnetti, S. M., Mendis, K. N. & David, P. H. (1987). Antigenic variation of cloned Plasmodium fragile in its natural host Macaco sinica. Sequential appearance of successive variant antigenic types. Journal of Experimental Medicine 165, 1269–83.Google Scholar
Helmby, H., Cavelier, L., Pettersson, U. & Wahlgren, M. (1993). Resetting Plasmodium falciparum-infected erythrocytes express unique strain-specific antigens on their surface. Infection and Immunity 61, 284–8.Google Scholar
Hommel, M., David, P. H. & Olgino, L. D. (1983). Surface alterations of erythrocytes infected with Plasmodium falciparum: antigenic variation and the role of the spleen. Journal of Experimental Medicine 157, 1137–48.Google Scholar
Howard, R. J., Barnwell, J. W. & Kao, V. (1983). Antigenic variation in Plasmodium knowlesi malaria: identification of the variant antigen on the surface of infected erythrocytes. Proceedings of the National Academy of Sciences, USA 80, 4129–33.CrossRefGoogle ScholarPubMed
Howard, R. J., Handunnetti, S. M., Hasler, T., Gilladoga, A., de Aguiar, J. C., Pasloske, B. L., Morehead, K., Albrecht, G. R. & Schravendijk, Van M. R. (1990). Surface molecules on Plasmodium falciparum-infected erythrocytes involved in adherence. American Journal of Tropical Medicine and Hygiene 43, 1529.CrossRefGoogle ScholarPubMed
Johnson, J. K., Swerlick, R. A., Grady, K. K., Millet, P. & Wick, T. M. (1993). Cytoadherence of Plasmodium falciparum-infected erythrocytes to microvascular endothelium is regulatable by cytokines and phorbol ester. Journal of Infectious Diseases 167, 698703.Google Scholar
Kaul, D. K., Roth, E. Jr., Nagel, R. L., Howard, R. J. & Handunnetti, S. M. (1991). Resetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78, 812–19.CrossRefGoogle Scholar
Kilejian, A. (1979). Characterisation of a protein correlated with the production of knob-like protrusions on membranes of erythrocytes infected with Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 76, 4650–3.Google Scholar
Knowles, D. M., Tolidjan, B., Marboe, C., D'Agati, V., Grimes, M. & Chess, L. (1984). Monoclonal anti-human monocyte antibodies OKM1 and OKM5 possess distinctive tissue distribution including differential reactivity with vascular endothelium. Journal of Immunology 132, 2170–3.CrossRefGoogle Scholar
Kutner, S., Breuer, W. V., Ginsburg, H., Aley, S. B. & Cabantchik, Z. I. (1985). Characterization of permeation pathways in the plasma membrane of human erythrocytes infected with early stages of Plasmodium falciparum: association with parasite development. Journal of Celt Physiology 125, 521–7.Google Scholar
Kwiatkowski, D. (1990). Tumour necrosis factor, fever and fatality in falciparum malaria. Immunology Letters 25, 213–16.CrossRefGoogle ScholarPubMed
Kwiatkowski, D., Hill, A. V., Sambou, I., Twumasi, P., Castracane, J., Mamogue, K. R., Cerami, A., Brewster, D. R. & Greenwood, B. M. (1990). TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336, 1201–4.CrossRefGoogle ScholarPubMed
Leech, J. H., Barnwell, J. W., Miller, L. H. & Howard, R. J. (1984). Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. Journal of Experimental Medicine 159, 1567–75.Google Scholar
MacPherson, G. G., Warrell, M. J., White, N. J., Looareesuwan, S. & Warrell, D. A. (1985). Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. American Journal of Pathology 119, 385401.Google ScholarPubMed
Magowan, C., Wollish, W., Anderson, L. & Leech, J. (1988). Cytoadherence by Plasmodium falciparum-infected erythrocytes is correlated with the expression of a family of variable proteins on infected erythrocytes. Journal of Experimental Medicine 168, 1307–20.CrossRefGoogle ScholarPubMed
Marsh, K. & Howard, R. J. (1986). Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science 231, 150–3.Google Scholar
Marsh, K., Marsh, V. M., Brown, J., Whittle, H. C. & Greenwood, B. M. (1988). Plasmodium falciparum: the behavior of clinical isolates in an in vitro model of infected red blood cell sequestration. Experimental Parasitology 65, 202–8.Google Scholar
Miller, L. H. (1969). Distribution of mature trophozoites and schizonts of Plasmodium falciparum in the organs of Aotus trivirgatus, the night monkey. American Journal of Tropical Medicine and Hygiene 18, 860–5.Google Scholar
Nakamura, K., Hasler, T., Morehead, K., Howard, R. J. & Aikawa, M. (1992). Plasmodium falciparum infected erythrocyte receptor(s) for CD36 and thrombospondin are restricted to knobs on the erythrocyte surface. Journal of Histochemistry and Cytochemistry 40, 1419–22.CrossRefGoogle ScholarPubMed
Nash, G. B., Cooke, B. M., Marsh, K., Berendt, A., Newbold, C. & Stuart, J. (1992). Rheological analysis of the adhesive interactions of red blood cells parasitized by Plasmodium falciparum. Blood 79, 798807.CrossRefGoogle ScholarPubMed
Newbold, C. I., Pinches, R., Roberts, D. J. & Marsh, K. (1992). Plasmodium falciparum: the human agglutinating antibody response to the infected red cell surface is predominantly variant specific. Experimental Parasitology 75, 281–92.CrossRefGoogle Scholar
Ockenhouse, C. F., Betageri, R., Springer, T. A. & Staunton, D. E. (1992 a). Plasmodium falciparum-infected erythrocytes bind ICAM-1 at a site distinct from LFA-1, Mac-1, and human rhinovirus [published erratum appears in Cell (1992) 68: following 994]. Cell 68, 63–9.CrossRefGoogle Scholar
Ockenhouse, C. F., Klotz, F. W., Tandon, N. N. & Jamieson, G. A. (1991). Sequestrin, a CD36 recognition protein on Plasmodium falciparum malaria-infected erythrocytes identified by anti-idiotype antibodies. Proceedings of the National Academy of Sciences, USA 88, 3175–9.CrossRefGoogle ScholarPubMed
Ockenholuse, C. F., Tandon, N. N., Magowan, C., Jamieson, C. A. & Chulay, J. D. (1989). Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor [see comments]. Science 243, 1469–71.CrossRefGoogle Scholar
Ockenhouse, C. F., Tegoshi, T., Maeno, Y., Benjamin, C., Ho, M., Kan, K. E., Thway, Y., Win, K., Aikawa, M. & Lobb, R. R. (1992 b). Human vascular endothelial cell adhesion receptors for Plasmodium falciparum-infected erythrocytes: roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1. Journal of Experimental Medicine 176, 1183–9.Google Scholar
Oquendo, P., Hundt, E., Lawler, J. & Seed, B. (1989). CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 58, 95101.CrossRefGoogle ScholarPubMed
Osborn, L., Hession, C., Tizard, R., Vassallo, C., Luhowskyj, S., Chi-Rosso, G. & Lobb, R. (1989). Direct expression cloning of Vascular Cell Adhesion Molecule 1, a cytokine induced endothelial protein that binds to lymphocytes. Cell 59, 1203–11.Google Scholar
Roberts, D. D., Sherwood, J. A., Spitalnik, S. L., Panton, L. J., Howard, R. J., Dixit, V. M., Frazier, W. A., Miller, L. H. & Ginsburg, V. (1985). Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature 318, 64–6.Google Scholar
Roberts, D. J., Biggs, B.-A., Brown, G. & Newbold, C. I. (1993). Protection, pathogenesis and phenotypic plasticity in Plasmodium falciparum malaria. Parasitology Today 9, 281–6.CrossRefGoogle ScholarPubMed
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 [see comments]. Nature 357, 689–92.CrossRefGoogle ScholarPubMed
Rowe, A., Berendt, A. R., Marsh, K. & Newbold, C. I. (1994). Plasmodium falciparum: A family of sulphated glycoconjugates disrupt erythrocyte rosettes. Experimental Parasitology, in press.CrossRefGoogle ScholarPubMed
Sherwood, J. A., Roberts, D. D., Spitalnik, S. L., Marsh, K., Harvey, E. B., Miller, L. H. & Howard, R. J. (1989). Studies of the receptors on melanoma cells for Plasmodium falciparum infected erythrocytes. American Journal of Tropical Medicine and Hygiene 40, 119–27.CrossRefGoogle ScholarPubMed
Treutiger, C. J., Hedlund, I., Helmby, H., Carlson, J., Jepson, A., Twumasi, P., Kwiatkowski, D., Greenwood, B. M. & Wahlgren, M. (1992). Rosette formation in Plasmodium falciparum isolates and antirosette activity of sera from Gambians with cerebral or uncomplicated malaria. American Journal of Tropical Medicine and Hygiene 46, 503–10.CrossRefGoogle ScholarPubMed
Udeinya, I. J., Leech, J., Aikawa, M. & Miller, L. H. (1985). An in vitro assay for sequestration: binding of Plasmodium falciparum-infected erythrocytes to formalin-fixed endothelial cells and amelanotic melanoma cells. Journal of Protozoology 32, 8890.CrossRefGoogle Scholar
Udeinya, I. J., Miller, L. H., McGregor, I. A. & Jensen, J. B. (1983). Plasmodium falciparum strain specific antibody blocks binding of infected erythrocytes to amelanotic melanoma cells. Nature 303, 429–31.CrossRefGoogle ScholarPubMed
Warrell, D. A. (1987). Pathophysiology of severe falciparum malaria in man. Parasitology 94, S5376.CrossRefGoogle ScholarPubMed
White, N. J., Warrell, D. A., Looareesuwan, S., Chanthavanich, P., Phillips, R. E. & Pongpaew, P. (1985). Pathophysiological and prognostic significance of cerebrospinal-fluid lactate in cerebral malaria. Lancet 1, 776–8.CrossRefGoogle ScholarPubMed
Wick, T. M. & Louis, V. (1991). Cytoadherence of Plasmodium falciparum-infected erythrocytes to human umbilical vein and human dermal microvascular endothelial cells under shear conditions. American Journal of Tropical Medicine and Hygiene 45, 578–86.Google Scholar