Hostname: page-component-77c89778f8-gvh9x Total loading time: 0 Render date: 2024-07-17T09:09:52.509Z Has data issue: false hasContentIssue false
  • English
  • Français

Cytoadherence of knobby and knobless Plasmodium falciparum-infected erythrocytes

Published online by Cambridge University Press:  06 April 2009

W. Ruangjirachuporn ,
B. A. Afzelius ,
S. Paulie ,
M. Wahlgren ,
K. Berzins  and
P. Perlmann
W. Ruangjirachuporn
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden Department of Ultrastructure Research, Stockholm University, S-106 91 Stockholm, Sweden
B. A. Afzelius
Affiliation:
Department of Ultrastructure Research, Stockholm University, S-106 91 Stockholm, Sweden
S. Paulie
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
M. Wahlgren
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
K. Berzins
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
P. Perlmann
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
Get access Rights & Permissions [Opens in a new window]

Extract

Cytoadherence of Plasmodium falciparum-infected erythrocytes to melanoma cells was analysed using strains or isolates of parasites expressing or not expressing knobs (K+ or K− phenotype) on the erythrocyte surface. Both K+ and K− parasites had the capacity to cytoadhere to melanoma cells. Using a panel of melanoma cell lines with different surface expression of the cytoadherence receptors CD36, thrombospondin and ICAM-1 indicated that CD36 was the major receptor for parasites of both K+ and K− phenotypes. Binding competition experiments between K+ and K−-infected erythrocytes suggested that K+ cytoadherence is of higher affinity than that of K− parasites. However, some K− cytoadherence was also found in isolates containing mixed populations of K+ and K− parasites. The interaction of the two types of infected erythrocytes with melanoma cells also differed ultrastructurally, erythrocytes of K+ phenotype showing intimate interdigitations with microvilli on the melanoma cells, while erythrocytes of K− phenotype displayed more separated interactions with fewer sites of contact and involving only a few melanoma cell microvilli. One and the same infected erythrocyte may co-express the ligand for CD36-mediated cytoadherence and the structures mediating binding of uninfected erythrocytes to form rosettes.

Keywords

Plasmodium falciparumcytoadherencemelanoma cellsknobserythrocytesrosetting
Type
Research Article
Information
Parasitology , Volume 102 , Issue 3 , June 1991 , pp. 325 - 334
Copyright
Copyright © Cambridge University Press 1991

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

Aikawa, M. (1988). Human cerebral malaria. American Journal of Tropical Medicine and Hygiene 39, 3–10.Google Scholar
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.Google Scholar
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., 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, London 341, 57–9.Google Scholar
Biggs, B. A., Culvenor, J. G., Ng, J. S., Kemp, D. J. & Brown, G. V. (1989 a). Plasmodium falciparum: Cytoadherence of a knobless clone. Experimental Parasitology 69, 189–97.Google Scholar
Biggs, B. A., Gooze, L., Wycherley, K., Wilkinson, D., Boyd, A. W., Forsyth, K. P., Edelman, L., Brown, G. V. & Leech, J. H. (1990). Knob-independent cytoadherence of Plasmodium falciparum to the leukocyte differentiation antigen CD36. Journal of Experimental Medicine 171, 1883–92.Google Scholar
Biggs, B. A., Kemp, D. J. & Brown, G. V. (1989 b). Subtelomeric chromosome deletions in field isolates of Plasmodium falciparum and their relationship to loss of cytoadherence in vitro. Proceedings of the National Academy of Sciences, USA 86, 2428–32.Google Scholar
Bruning, J. W., Kardol, M. J. & Arentzen, R. (1980). Carboxyfluorescein fluorochromasia assays. I. Non-radioactively labeled cell mediated lympholysis. Journal of Immunological Methods 33, 33–44.Google Scholar
Carlson, J., Helmby, H., Hill, A. V. S., Brewster, D., Greenwood, B. M. & Wahlgren, M. (1990). Human cerebral malaria: association with erythrocyte rosetting and the lack of anti-rosetting antibodies. Lancet (in the Press.)Google Scholar
Corbett, C. E. P., Duarte, M. I. S., Lancellotti, C. L. P., Silva, M. A. I. G. & Andrade, H. F. Jr (1989). Cytoadherence in human falciparum malaria as a cause of respiratory distress. Journal of Tropical Medicine and Hygiene 92, 112–20.Google 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.Google Scholar
Hommel, M. & Semoff, S. (1988). Expression and function of erythrocyte-associated surface antigens in malaria. Biology of the Cell 64, 183–203.Google Scholar
Howard, R. J. (1988). Malarial proteins at the membrane of Plasmodium falciparum-infected erythrocytes and their involvement in cytoadherence to endothelial cells. Progress in Allergy 41, 98–147.Google Scholar
Howard, R. J. & Gilladoga, A. D. (1989). Molecular studies related to the pathogenesis of cerebral malaria. Blood 74, 2603–18.CrossRefGoogle Scholar
Jaffe, E. A., Ruggiero, J. T., Leung, L. L. K., Doyle, M. J., McKeown-Longo, P. J. & Mosher, D. F. (1983). Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix. Proceedings of the National Academy of Sciences, USA 80, 998–1002.Google Scholar
Kilejian, A., Abati, A. & Trager, W. (1977). Plasmodium falciparum and Plasmodium coatneyi immunogenicity of ‘knob-like protrusions’ on infected erythrocyte membranes. Experimental Parasitology 42, 157–64.Google Scholar
Lampson, L. A. & Levy, R. (1980). Two populations of Ia-like molecules on a human B cell line. Journal of Immunology 125, 293–9.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, 443–52.CrossRefGoogle ScholarPubMed
Langreth, S. G. & Peterson, E. (1985). Pathogenicity, stability, and immunogenicity of a knobless clone of Plasmodium falciparum in Colombian owl monkeys. Infection and Immunity 47, 760–6.Google Scholar
Langreth, S. G. & Reese, R. T. (1977). Antigenicity of the infected erythrocyte and merozoite surfaces in falciparum malaria. Journal of Experimental Medicine 150, 1241–54.Google Scholar
Langreth, S. G., Reese, R. T., Motyl, M. R. & Trager, W. (1979). Plasmodium falciparum: Loss of knobs on the infected erythrocyte surface after long-term cultivation. Experimental Parasitology 48, 313–19.Google Scholar
Leech, J. H., Barnwell, J. W., Aikawa, M., Miller, L. H. & Howard, R. J. (1984). Plasmodium falciparum malaria: Association of knobs on the surface of infected erythrocytes with a histidine-rich protein and the erythrocyte skeleton. Journal of Cell Biology 98, 1256–64.CrossRefGoogle ScholarPubMed
Luse, S. A. & Miller, L. H. (1971). Plasmodium falciparum malaria. Ultrastructure of parasitized erythrocytes in cardiac vessels. American Journal of Tropical Medicine and Hygiene 20, 655–60.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, 385–401.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
Ockenhouse, C. F., Tandon, N. N., Magowan, C., Jamieson, G. A. & Chulay, J. D. (1989). Identification of a platelet membrane glycoprotein as a falciparum malaria sequestrian receptor. Science 243, 1469–71.Google Scholar
Panton, L. J., Leech, J. H., Miller, L. H. & Howard, R. J. (1987). Cytoadherence of Plasmodium falciparum-infected erythrocytes to human melanoma cell lines correlates with surface OKM5 antigen. Infection and Immunity 55, 2754–8.Google Scholar
Perlmann, H., Berzins, K., Wahlgren, M., Carlsson, J., Björkman, A., Patarroyo, M. E. & Perlmann, P. (1984). Antibodies in malarial sera to parasite antigens in the membranes of erythrocytes infected with early asexual stages of Plasmodium falciparum. Journal of Experimental Medicine 159, 1686–704.CrossRefGoogle ScholarPubMed
Raventos-Suarez, C., Kaul, D. K., Macaluso, F. & Nagel, R. L. (1985). Membrane knobs are required for the microcirculatory obstruction induced by Plasmodium falciparum-infected erythrocytes. Proceedings of the National Academy of Sciences, USA 82, 3829–33.Google Scholar
Riganti, M., Pongponratn, E., Tegoshi, T., Looareesuwan, S., Punpoowong, B. & Aikawa, M. (1990). Human cerebral malaria in Thailand: a clinico-pathological correlation. Immunological Letters 25, 199–206.Google Scholar
Roberts, D. D., Sherwood, J. A., Spitalnik, S. L., Panton, L. J., Howard, R. J., Dixit, V. M., Fazier, W. A., Miller, L. H. & Ginsburg, V. (1985). Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature, London 318, 64–6.Google Scholar
Rock, E. P., Roth, E. F. Jr, Rojas-Corona, R. R., Sherwood, J. A., Nagel, R. L., Howard, R. J. & Kaul, D. K. (1988). Thrombospondin mediates the cytoadherence of Plasmodium falciparum-infected red cells to vascular endothelium in shear flow conditions. Blood 71, 71–5.Google Scholar
Schulz, T. F., Mitterer, M., Neumayer, H. P., Vogetseder, W. & Dierich, M. P. (1988). Involvement in the initiation of T cell responses and structural features of an 85-kDa membrane activation antigen. European Journal of Immunology 18, 1253–8.Google Scholar
Sherwood, J. A., Roberts, D. D., Marsh, K., Harvey, E. B., Spitalnik, S. L., Miller, L. H. & Howard, R. J. (1987). Thrombospondin binding by parasitized erythrocytes isolates in falciparum malaria. American Journal of Tropical Medicine and Hygiene 36, 228–33.Google Scholar
Sherwood, J. A., Roberts, D. D., Spitalnik, S. L., Lawler, J. W., Miller, L. H. & Howard, R. J. (1990). Falciparum malaria parasitized erythrocytes bind to a carboxy-terminal thrombospondin fragment and not the amino-terminal heparin-binding region. Molecular and Biochemical Parasitology 40, 173–82.Google Scholar
Taylor, D. W., Parra, M., Chapman, G. B., Stearns, M. D., Rener, J., Aikawa, M., Uni, S., Aley, S. B., Panton, L. J. & Howard, R. J. (1987). Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs. Molecular and Biochemical Parasitology 25, 165–74.Google Scholar
Taylor, D. W., Parra, M. & Stearns, M. E. (1987). Plasmodium falciparum: Fine structural changes in the cytoskeletons of infected erythrocytes. Experimental Parasitology 64, 178–87.Google Scholar
Trager, W. & Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.Google Scholar
Trager, W., Rudzinska, M. A. & Bradbury, P. C. (1966). The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infection in man. Bulletin of the World Health Organization 35, 883–5.Google Scholar
Udeinya, I. J., Graves, P. M., Carter, R., Aikawa, M. & Miller, L. H. (1983). Plasmodium falciparum: Effect of time in continuous culture on binding to human endothelial cells and melanotic melanoma cells. Experimental Parasitology 56, 207–14.Google Scholar
Udomsangpetch, R., Aikawa, M., Berzins, K., Wahlgren, M. & Perlmann, P. (1989 a). Cytoadherence of knobless Plasmodium falciparum-infected erythrocytes and its inhibition by a human monoclonal antibody. Nature, London 338, 763–5.Google Scholar
Udomsangpetch, R., Carlsson, J., Wåhlin, B., Holmquist, G., Ozaki, L. S., Scherf, A., Mattei, D., Mercereau-Puijalon, O., Uni, S., Aikawa, M., Berzins, K. & Perlmann, P. (1989 b). Reactivity of the human monoclonal antibody 33G2 with repeated sequences of three distinct Plasmodium falciparum antigens. Journal of Immunology 142, 3620–6.Google Scholar
Udomsangpetch, R., Wåhlin, B., Carlson, J., Berzins, K., Torii, M., Aikawa, M., Perlmann, P. & Wahlgren, M. (1989 c). Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. Journal of Experimental Medicine 169, 1835–40.Google Scholar
Wahlgren, M., Carlson, J., Udomsangpetch, R. & Perlmann, P. (1989). Why do Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes? Parasitology Today 5, 183–5.Google Scholar