Hostname: page-component-84b7d79bbc-x5cpj Total loading time: 0 Render date: 2024-07-26T02:12:22.192Z Has data issue: false hasContentIssue false
  • English
  • Français

Adhesion of parasitized red blood cells to cultured endothelial cells: a flow-based study of isolates from Gambian children with falciparum malaria

Published online by Cambridge University Press:  06 April 2009

B. M. Cooke ,
S. Morris-Jones ,
B. M. Greenwood  and
G. B. Nash
B. M. Cooke
Affiliation:
Department of Haematology, The Medical School, University of Birmingham, Birmingham B15 2TT, UK
S. Morris-Jones
Affiliation:
The Medical Research Council Laboratories, P.O. Box 273, Fajara, Nr Banjul, The Gambia, West Africa
B. M. Greenwood
Affiliation:
The Medical Research Council Laboratories, P.O. Box 273, Fajara, Nr Banjul, The Gambia, West Africa
G. B. Nash
Affiliation:
Department of Haematology, The Medical School, University of Birmingham, Birmingham B15 2TT, UK
Get access Rights & Permissions [Opens in a new window]

Summary

Adhesion of parasitized red blood cells to vascular endothelium is thought to play an important role in the development of the ischaemic complications associated with severe falciparum malaria. Using a novel, flow-based assay, we have investigated the adhesion of parasitized red blood cells to formalin-fixed human umbilical vein endothelial cells (HUVEC), for isolates obtained from 32 Gambian subjects with mild or severe falciparum malaria. Red cells infected with wild strains of Plasmodium falciparum were able to adhere to HUVEC under physiologically relevant flow conditions, but the level of adhesion was highly variable, ranging from 1 to 688 adherent cells per mm2 of HUVEC. Within isolates, some adherent parasitized cells remained stationary, whilst other formed less stable interactions and rolled slowly over the cell surface. There was no significant difference in adhesion of parasitized cells between isolates obtained from mild or severe cases of malaria, although a subset of isolates did show very high levels of adhesion. The results suggest that there is not a simple relationship between the adhesion of parasitized cells to cultured endothelial cells (presumably via the receptor ICAM-1) and the clinical severity of the disease, although variation in microvascular adhesion in vivo may still be a determinant of ischaemic complications.

Keywords

malariaerythrocytesadhesionendothelial cellsrheology
Type
Research Article
Information
Parasitology , Volume 107 , Issue 4 , November 1993 , pp. 359 - 368
Copyright
Copyright © Cambridge University Press 1993

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. (1988). Human cerebral malaria. American Journal of Tropical Medicine and Hygiene 39, 3–10.CrossRefGoogle ScholarPubMed
Aikawa, M., Iseki, M., Barnwell, J. W., Taylor, D., OO, M. M. & Howard, R. J. (1990). The pathology of human cerebral malaria. American Journal of Tropical Medicine and Hygiene 43, 30–7.CrossRefGoogle ScholarPubMed
Atherton, A. & Born, G. V. R. (1972). Quantitative investigations of the adhesiveness of circulating polymorphonuclear leucocytes to blood vessel walls. Journal of Physiology 222, 447–74.CrossRefGoogle ScholarPubMed
Barabino, G. A., McIntire, L. V., Eskin, S. G., Sears, D. A. & Udden, M. (1987). Endothelial cell interactions with sickle cell, sickle trait, mechanically injured, and normal erythrocytes under controlled flow. Blood 70, 152–7.CrossRefGoogle ScholarPubMed
Barnwell, J. W. (1989). Cytoadherence and sequestration in falciparum malaria. Experimental Parasitology 69, 407–12.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., Ockenhouse, C. G. & Knowles, D. M. (1985). Monoclonal antibody OKM5 inhibits the in vitro binding of Plasmodium falciparum-infected 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.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, London 341, 57–9.CrossRefGoogle ScholarPubMed
Biggs, B., 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.CrossRefGoogle 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 lack of anti-rosetting antibodies. Lancet 336, 1457–60.CrossRefGoogle ScholarPubMed
Chien, S. (1987). Physiological and pathophysiological significance of haemorheology. In Clinical Haemorheology (ed. Chien, S., Dormandy, J., Ernst, E. & Matrai, A.), pp. 125–164. Dordrecht: Martinus Nijhoff.CrossRefGoogle Scholar
Cooke, B. M., Usami, S., Perry, I. & Nash, G. B. (1993). A simplified method for culture of endothelial cells and analysis of adhesion of blood cells under conditions of flow. Microvascular Research 45, 33–45.CrossRefGoogle ScholarPubMed
David, P. H., Hommel, M., Miller, L. H., Udeinya, I. J. & Oligiono, 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
Goldring, J. D., Molyneux, M. E., Taylor, T., Wirima, J. & Hommel, M. (1992). Plasmodium falciparum – diversity of isolates from Malawi in their cytoadherence to melanoma cells and monocytes in vitro. British Journal of Haematology 81, 413–18.CrossRefGoogle ScholarPubMed
Greenwood, B. M., Bradley, A. K., Greenwood, A. M., Byass, P., Jammeh, K., Marsh, K., Tulloch, S., Oldfield, F. S. J. & Hayes, R. (1987). Mortality and morbidity from malaria among children in a rural area of The Gambia, West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 478–86.CrossRefGoogle Scholar
Hasler, T., Handunnetti, S. M., Aguiar, J. C., Van Schravendijk, M. R., Greenwood, B. M., Lallinger, G., Cegielski, P. & Howard, R. J. (1990). In vitro rosetting, cytoadherence, and microagglutination properties of Plasmodium falciparum-infected erythrocytes from Gambian and Tanzanian patients. Blood 76, 1845–52.CrossRefGoogle ScholarPubMed
Ho, M., Davis, T. M. E., Silamut, K., Bunnag, D. & White, N. J. (1991 a). Rosette formation of Plasmodium falciparum-infected erythrocytes from patients with acute malaria. Infection and Immunity 59, 2135–9.CrossRefGoogle ScholarPubMed
Ho, M., Singh, B., Looareesuwan, S., Davis, T. M. E., Bunnag, D. & White, N. J. (1991 b). Clinical correlates of in vitro P. falciparum cytoadherence. Infection and Immunity 59, 873–8.CrossRefGoogle Scholar
Howard, R. J. & Gilladoga, A. D. (1989). Molecular studies related to the pathogenesis of cerebral malaria. Blood 74, 2603–18.CrossRefGoogle Scholar
Johnson, J. P., Stade, B. G., Holzmann, B., Schwable, W. & Riethmuller, G. (1989). De novo expression of intercellular-adhesion molecule 1 in melanoma correlates with increased risk of metastasis. Proceedings of the National Academy of Sciences, USA 86, 641–4.CrossRefGoogle ScholarPubMed
Klitzman, B. & Duling, B. R. (1979). Microvascular haematocrit and red cell flow in resting and contracting striated muscle. American Journal of Physiology 237, H481–90.Google ScholarPubMed
Lipowsky, H. H., Kovalchek, S. & Zweifach, B. W. (1978). The distribution of blood rheological parameters in the microcirculation of cat mesentery. Circulation Research 43, 738–49.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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Marsh, K., Marsh, V. M., Brown, J., Whittle, H. C. & Greenwood, B. M. (1988). Plasmodium falciparum: the behaviour of clinical isolates in an in vitro model of infected red blood cell sequestration. Experimental Parasitology 65, 202–8.CrossRefGoogle Scholar
Meryman, H. T. & Hornblower, M. (1972). A method for freezing and washing red blood cells using a high glycerol concentration. Transfusion 12, 145–56.CrossRefGoogle ScholarPubMed
Molyneux, M. E., Taylor, T. E., Wirima, J. J. & Borgstein, A. (1989). Clinical features and prognostic indicators in paediatric cerebral malaria: a study of 131 comatose Malawian children. Quarterly Journal of Medicine 265, 441–59.Google Scholar
Nash, B. B., Cooke, B. M., Marsh, K., Berendt, A., Newbold, C. & Stuart, J. (1992 a). Rheological analysis of the adhesive interactions of red blood cells parasitized by Plasmodium falciparum. Blood 79, 798–807.CrossRefGoogle ScholarPubMed
Nash, G. B., Cooke, B. M., Carlson, J. & Wahlgren, M. (1992 b). Rheological properties of rosettes formed by red blood cells parasitized by Plasmodium falciparum. British Journal of Haematology 82, 1–7.CrossRefGoogle ScholarPubMed
Nash, G. B., Cooke, B. M., Berendt, A., Craig, A. & Newbold, C. (1992 c). Roles of different receptors in cytoadhesion of red cells parasitized by Plasmodium falciparum. Blood 80 (Suppl. 1), 342a.Google Scholar
Ockenhouse, C. F., Ho, M., Tandon, N. N., Van Seventer, G. A., Shaw, S., White, N. J., Jamieson, G. A., Chulay, J. D. & Webster, H. K. (1991). Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: differential adhesion of infected erythrocytes to CD36 and ICAM-1. Journal of Infectious Diseases 164, 163–9.CrossRefGoogle ScholarPubMed
Ockenhouse, C. F., Tegoshit, T., Maeno, Y., Benjamin, C., Ho, M., Kan, K. E., Thway, Y., Win, K., Aikawa, M. & Lobb, R. R. (1992). 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.CrossRefGoogle ScholarPubMed
Oquendo, P., Hundt, E., Lawler, J. & Seed, B. (1989). CD36 directly mediates cytoadherence of Plasmodium falciparum parasitized erythrocytes. Cell 58, 95–101.CrossRefGoogle ScholarPubMed
Phillips, R. E. & Solomon, T. (1990). Cerebral malaria in children. Lancet 336, 1355–60.CrossRefGoogle ScholarPubMed
Pongponratn, E., Riganti, M., Punpoowong, B. & Aikawa, M. (1991). Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. American Journal of Tropical Medicine and Hygiene 44, 168–75.CrossRefGoogle ScholarPubMed
Raventos-Suarez, C., Kaul, D. K., Mascaluso, 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.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. Nature, London 357, 689–92.CrossRefGoogle ScholarPubMed
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, London 318, 64–6.CrossRefGoogle ScholarPubMed
Rock, E. P., Roth, E. F. Jr, Rojas-Corona, R. R., Sherwood, J. A., Nagel, R. L., Howard, R. N. & 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.CrossRefGoogle ScholarPubMed
Sherman, I. W., Crandall, I. & Smith, H. (1992). Membrane proteins involved in the adherence of Plasmodium falciparum-infected erythrocytes to the endothelium. Biology of the Cell 74, 161–78.CrossRefGoogle ScholarPubMed
Swerlick, R. A., Lee, K. H., Wick, T. M. & Lawley, T. J. (1992). Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. Journal of Immunology 148, 78–83.CrossRefGoogle Scholar
Trager, W. & Jensen, B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.CrossRefGoogle ScholarPubMed
Trager, W., Rudzinska, M. A. & Bradbury, P. C. (1986). The fine structure of Plasmodium falciparum and its host erythrocytes in natural malarial infections in man. Bulletin of the World Health Organization 35, 883–5.Google Scholar
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
Udomsangpetch, R., Wahlin, B., Carlson, J., Berzins, K., Torii, M., Aikawa, M., Perlmann, P. & Wahlgren, M. (1989). Plasmodium falciparum-infected erythrocytes form spontaneous erythrocyte rosettes. Journal of Experimental Medicine 169, 1835–40.CrossRefGoogle ScholarPubMed
Warrell, D. A., Looareesuwan, S., Warrell, M. J., Kasemsarn, P., Intaraprasert, R., Bunnag, D. & Harinasuta, T. (1982). Dexamethasone proves deleterious in cerebral malaria. New England Journal of Medicine 306, 313–19.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.CrossRefGoogle ScholarPubMed
World Health Organization Malaria Action Programme (1986). Severe and complicated malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 3–50.CrossRefGoogle Scholar