Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells

EMBO Journal

Volumn 19, Issue 12, 2000, Pages 2813-2823

  Waterkeyn, Jacqueline G ^c   Wickham, Mark E ^c   Davern, Kathleen M ^c   Cooke, Brian M ^a   Coppel, Ross L ^a   Reeder, John C ^c   Culvenor, Janetta G ^b   Waller, Ross F ^b   Cowman, Alan F ^c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Cytoadherence; Malaria; PfEMP1; PfEMP3; Protein trafficking

Indexed keywords

MEMBRANE PROTEIN;

ARTICLE; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; ERYTHROCYTE MEMBRANE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MALARIA; MUTAGENESIS; PATHOGENESIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN TRANSPORT;

PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 0034660256     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.12.2813     Document Type: Article

References (30)

1. Baruch, D.I., Pasloske, B.L., Singh, H.B., Bi, X., Ma, X.C., Feldman, M., Taraschi, T.F. and Howard, R.J. (1995) Cloning the P.falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell, 82, 77-87.
2. Baruch, D.I., Gormley, J.A., Ma, C., Howard, R.J. and Pasloske, B.L. (1996) Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin and intercellular adhesion molecule I. Proc. Natl Acad Sci. USA, 93, 3497-3502.
3. Baruch, D.I., Ma, X.C., Singh, H.B., Bi, X., Pasloske, B.L. and Howard, R.J. (1997) Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. Blood, 90, 3766-3775.
4. Cao, X., Ballew, N. and Barlowe, C. (1998) Initial docking of ER-derived vesicles required Usolp and Yptlp but is independent of SNARE proteins. EMBO J., 17, 2156-2165.
5. Chu, G., Vollrath, D. and Davis, R. (1986) Separation of large DNA molecules by contour clamped homogeneous electric fields. Science, 234, 1582-1585.
6. Cooke, B.M., Berendt, A.R., Craig, A.G., MacGregor, J., Newbold, C.I. and Nash, G.B. (1994) Rolling and stationary cytoadhesion of red blood cells parasitized by Plasmodium falciparum: separate roles for ICAM-1. CD36 and thrombospondin. Br. J. Haematol., 87, 162-170.
7. Corcoran, L.M., Forsyth, K.P., Bianco, A.E., Brown, G.V. and Kemp, D.J. (1986) Chromosome size polymorphisms in Plasmodium falciparum can involve deletions and are frequent in natural parasite populations. Cell, 44, 87-95.
8. Cowman, A.F., Karcz, S., Galatis, D. and Culvenor, J.G. (1991) A P-glycoprotein homologue of Plasmodium falciparum is localized on the digestive vacuole. J. Cell Biol., 113, 1033-1042.
9. Crabb, B.S. and Cowman, A.F. (1996) Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 93, 7289-7294.
10. Crabb, B.S. et al. (1997a) Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell, 89, 287-296.
11. Crabb, B.S., Triglia, T., Waterkeyn, J.G. and Cowman, A.F. (1997b) Stable transgene expression in Plasmodium falciparum. Mol. Biochem. Parasitol., 90, 131-144.
12. Culvenor, J.G., Langford, C.J., Crewther, P.E., Saint, R.B., Coppel, R.L., Kemp, D.J., Anders, R.F. and Brown, G.V. (1987) Plasmodium falciparum: identification and localization of a knob protein antigen expressed by a cDNA clone. Exp. Parasitol., 63, 58-67.
13. Deitsch, K.W. and Wellems, T.E. (1996) Membrane modifications in erythrocytes parasitized by Plasmodium falciparum. Mol. Biochem. Parasitol., 76, 1-10.
14. Gardner, J.P., Pinches, R.A., Roberts, D.J. and Newbold, C.I. (1996) Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 93, 3503-3508.
15. Gardner, M.J. et al. (1998) Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Science, 282, 1126-1132.
16. Kyes, S., Taylor, H., Craig, A., Marsh, K. and Newbold, C. (1997) Genomic representation of var gene sequences in Plasmodium falciparum field isolates from different geographic regions. Mol. Biochem. Parasitol., 87, 235-238.
17. Leech, J.H., Barnwell, J.W., Miller, L.H. and Howard, R.J. (1984) Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. J. Exp. Med., 159, 1567-1575.
18. MacPherson, G.G., Warrell, M.J., White, N.J., Looareesuwan, S. and Warrell, D.A. (1985) Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am. J. Pathol., 119, 385-401.
19. Nakajima, H., Hirata, A., Ogawa, Y., Yonehara, T., Yoda, K. and Yamasaki, M. (1991) A cytoskeleton-related gene, USOI, is required for intracellular protein transport in Saccharomyces cerevisiae. J. Cell. Biol., 113, 245-260.
20. Pasloske, B.L., Baruch, D.I., Van Schravendijk, M.R., Handunnetti, S.M., Aikawa, M., Fujioka, H., Taraschi, T.F., Gormley, J.A. and Howard, R.J. (1993) Cloning and characterization of a Plasmodium falciparum gene encoding a novel high-molecular weight host membrane-associated protein, PfEMP3. Mol. Biochem. Parasitol., 59, 59-72.
21. Pologe, L.G., Pavlovec, A., Shio, H. and Ravetch, J.V. (1987) Primary structure and subcellular localization of the knob-associated histidinerich protein of Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 84, 7139-7143.
22. Reeder, J.C., Cowman, A.F., Davern, K.M., Beeson, J.G., Thompson, J.K., Rogerson, S.J. and Brown, G.V. (1999) The adhesion of Plasmodium falciparum-infected erythrocytes to chondroitin sulfate A is mediated by PfEMP1. Proc. Natl Acad. Sci. USA, 96, 5198-5202.
23. Shulman, M., Wilde, C.D. and Köhler, G. (1978) A better cell line for making hybridomas secreting antibodies. Nature, 276, 269-270.
24. Smith, D.B. and Johnson, K.S. (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene, 67, 31-40.
25. Smith, J.D., Chitnis, C.E., Craig, A.G., Roberts, D.J., Hudson-Taylor, D.E., Peterson, D.S., Pinches, R., Newbold, C.I. and Miller, L.H. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell, 82, 101-110.
26. Su, X., Heatwole, V.M., Wertheimer, S.P., Guinet, F., Herrfeldt, J.A., Peterson, D.S., Ravetch, J.A. and Wellems, T.E. (1995) The large diverse gene family var encodes proteins involved in cyloadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell, 82, 89-100.
27. Trager, W. and Jensen, J.B. (1977) Cultivation of erythrocytic stages. Bull. WHO, 55, 363-365.
28. Triglia, T., Wang, P., Sims, P.F.G., Hyde, J.E. and Cowman, A.F. (1998) Allelic exchange at the endogenous genomic locus in Plasmodium falciparum proves the role of dihydropteroate synthase in sulfadoxine-resistant malaria. EMBO J., 17, 3807-3815.
29. Wu, Y., Sifri, C.D., Lei, H.-H., Su, X.-S. and Wellems, T.E. (1995) Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl Acad. Sci. USA, 92, 973-977.
30. 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. Proc. Natl Acad. Sci. USA, 93, 1130-1134.