Identification of a role for the PfEMP1 semi-conserved head structure in protein trafficking to the surface of Plasmodium falciparum infected red blood cells

Cellular Microbiology

Volumn 12, Issue 10, 2010, Pages 1446-1462

  Melcher, Martin ^a   Muhle, Rebecca A ^b,c   Henrich, Philipp P ^c   Kraemer, Susan M ^a   Avril, Marion ^a   Vigan Womas, Ines ^d   Mercereau Puijalon, Odile ^d   Smith, Joseph D ^a,e   Fidock, David A ^c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c NewYork Presbyterian Hospital   (United States)

^d CNRS   (France)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; INTEGRASE; PROTEIN BXB1; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL SURFACE; CYTOPLASM; ERYTHROCYTE; FLOW CYTOMETRY; HOST CELL; IMMUNITY; IMMUNOELECTRON MICROSCOPY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTEIN VARIANT; TRANSGENE;

CELL MEMBRANE; CONSERVED SEQUENCE; ERYTHROCYTES; FLOW CYTOMETRY; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MICROSCOPY, IMMUNOELECTRON; PLASMODIUM FALCIPARUM; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS;

PLASMODIUM FALCIPARUM;

EID: 77957115434     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01481.x     Document Type: Article

References (60)

1. Andrews, K.T., Pirrit, L.A., Przyborski, J.M., Sanchez, C.P., Sterkers, Y., Ricken, S., et al. (2003) Recovery of adhesion to chondroitin-4-sulphate in Plasmodium falciparum varCSA disruption mutants by antigenically similar PfEMP1 variants. Mol Microbiol 49: 655-669.
2. Avril, M., Kulasekara, B.R., Gose, S.O., Rowe, C., Dahlback, M., Duffy, P.E., et al. (2008) Evidence for globally shared, cross-reacting polymorphic epitopes in the pregnancy-associated malaria vaccine candidate VAR2CSA. Infect Immun 76: 1791-1800.
3. Baruch, D.I., Pasloske, B.L., Singh, H.B., Bi, X., Ma, X.C., Feldman, M., et al. (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.
4. 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.
5. Boddey, J.A., Moritz, R.L., Simpson, R.J., and Cowman, A.F. (2009) Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10: 285-299.
6. Chang, H.H., Falick, A.M., Carlton, P.M., Sedat, J.W., DeRisi, J.L., and Marletta, M.A. (2008) N-terminal processing of proteins exported by malaria parasites. Mol Biochem Parasitol 160: 107-115.
7. Chen, Q., Barragan, A., Fernandez, V., Sundstrom, A., Schlichtherle, M., Sahlen, A., et al. (1998) Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 187: 15-23.
8. Cooke, B.M., Buckingham, D.W., Glenister, F.K., Fernandez, K.M., Bannister, L.H., Marti, M., et al. (2006) A Maurer's cleft-associated protein is essential for expression of the major malaria virulence antigen on the surface of infected red blood cells. J Cell Biol 172: 899-908.
9. Elmendorf, H.G., Bangs, J.D., and Haldar, K. (1992) Synthesis and secretion of proteins by released malarial parasites. Mol Biochem Parasitol 52: 215-230.
10. Fidock, D.A., and Wellems, T.E. (1997) Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc Natl Acad Sci USA 94: 10931-10936.
11. Fidock, D.A., Nomura, T., and Wellems, T.E. (1998) Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase. Mol Pharmacol 54: 1140-1147.
12. Frank, M., and Deitsch, K. (2006) Activation, silencing and mutually exclusive expression within the var gene family of Plasmodium falciparum. Int J Parasitol 36: 975-985.
13. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
14. Gehde, N., Hinrichs, C., Montilla, I., Charpian, S., Lingelbach, K., and Przyborski, J.M. (2009) Protein unfolding is an essential requirement for transport across the parasitophorous vacuolar membrane of Plasmodium falciparum. Mol Microbiol 71: 613-628.
15. Hiller, N.L., Bhattacharjee, S., Van Ooij, C., Liolios, K., Harrison, T., Lopez-Estrano, C., and Haldar, K. (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306: 1934-1937.
16. Horrocks, P., Pinches, R., Christodoulou, Z., Kyes, S.A., and Newbold, C.I. (2004) Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci USA 101: 11129-11134.
17. Khunrae, P., Dahlback, M., Nielsen, M.A., Andersen, G., Ditlev, S.B., Resende, M., et al. (2010) Full-length recombinant Plasmodium falciparum VAR2CSA binds specifically to CSPG and induces potent parasite adhesion-blocking antibodies. J Mol Biol 397: 826-834.
18. Kilejian, A., Rashid, M.A., Aikawa, M., Aji, T., and Yang, Y.F. (1991) Selective association of a fragment of the knob protein with spectrin, actin and the red cell membrane. Mol Biochem Parasitol 44: 175-181.
19. Knuepfer, E., Rug, M., Klonis, N., Tilley, L., and Cowman, A.F. (2005) Trafficking of the major virulence factor to the surface of transfected P. falciparum-infected erythrocytes. Blood 105: 4078-4087.
20. De Koning-Ward, T.F., Gilson, P.R., Boddey, J.A., Rug, M., Smith, B.J., Papenfuss, A.T., et al. (2009) A newly discovered protein export machine in malaria parasites. Nature 459: 945-949.
21. Kraemer, S.M., and Smith, J.D. (2006) A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 9: 374-380.
22. Kraemer, S.M., Kyes, S.A., Aggarwal, G., Springer, A.L., Nelson, S.O., Christodoulou, Z., et al. (2007) Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8: 45.
23. Kriek, N., Tilley, L., Horrocks, P., Pinches, R., Elford, B.C., Ferguson, D.J., et al. (2003) Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Mol Microbiol 50: 1215-1227.
24. Kumar, N., Koski, G., Harada, M., Aikawa, M., and Zheng, H. (1991) Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Mol Biochem Parasitol 48: 47-58.
25. Lingelbach, K., and Przyborski, J.M. (2006) The long and winding road: protein trafficking mechanisms in the Plasmodium falciparum infected erythrocyte. Mol Biochem Parasitol 147: 1-8.
26. Lopez-Estrano, C., Bhattacharjee, S., Harrison, T., and Haldar, K. (2003) Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 100: 12402-12407.
27. Maier, A.G., Braks, J.A., Waters, A.P., and Cowman, A.F. (2006) Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol Biochem Parasitol 150: 118-121.
28. Maier, A.G., Rug, M., O'Neill, M.T., Beeson, J.G., Marti, M., Reeder, J., and Cowman, A.F. (2007) Skeleton-binding protein 1 functions at the parasitophorous vacuole membrane to traffic PfEMP1 to the Plasmodium falciparum-infected erythrocyte surface. Blood 109: 1289-1297.
29. Marti, M., Good, R.T., Rug, M., Knuepfer, E., and Cowman, A.F. (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306: 1930-1933.
30. Marti, M., Baum, J., Rug, M., Tilley, L., and Cowman, A.F. (2005) Signal-mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol 171: 587-592.
31. Miller, L.H., Baruch, D.I., Marsh, K., and Doumbo, O.K. (2002) The pathogenic basis of malaria. Nature 415: 673-679.
32. Muhle, R.A., Adjalley, S., Falkard, B., Nkrumah, L.J., Muhle, M.E., and Fidock, D.A. (2009) A var gene promoter implicated in severe malaria nucleates silencing and is regulated by 3' untranslated region and intronic cis-elements. Int J Parasitol 39: 1425-1439.
33. Nkrumah, L.J., Muhle, R.A., Moura, P.A., Ghosh, P., Hatfull, G.F., Jacobs, W.R., Jr, and Fidock, D.A. (2006) Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nature Methods 3: 615-621.
34. Oh, S.S., Voigt, S., Fisher, D., Yi, S.J., LeRoy, P.J., Derick, L.H., et al. (2000) Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the erythrocyte skeleton. Mol Biochem Parasitol 108: 237-247.
35. Roberts, D.J., Craig, A.G., Berendt, A.R., Pinches, R., Nash, G., Marsh, K., and Newbold, C.I. (1992) Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 357: 689-692.
36. Robinson, B.A., Welch, T.L., and Smith, J.D. (2003) Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Mol Microbiol 47: 1265-1278.
37. Rowe, J.A., Moulds, J.M., Newbold, C.I., and Miller, L.H. (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388: 292-295.
38. Salanti, A., Staalsoe, T., Lavstsen, T., Jensen, A.T., Sowa, M.P., Arnot, D.E., et al. (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49: 179-191.
39. Salanti, A., Dahlback, M., Turner, L., Nielsen, M.A., Barfod, L., Magistrado, P., et al. (2004) Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med 200: 1197-1203.
40. Saxton, W.O., Baumeister, W., and Hahn, M. (1984) Three-dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 13: 57-70.
41. Scherf, A., Hernandez-Rivas, R., Buffet, P., Bottius, E., Benatar, C., Pouvelle, B., et al. (1998) Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intraerythrocytic development in Plasmodium falciparum. EMBO J 17: 5418-5426.
42. Smith, J.D., Chitnis, C.E., Craig, A.G., Roberts, D.J., Hudson-Taylor, D.E., Peterson, D.S., et al. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101-110.
43. Smith, J.D., Kyes, S., Craig, A.G., Fagan, T., Hudson-Taylor, D., Miller, L.H., et al. (1998) Analysis of adhesive domains from the A4VAR Plasmodium falciparum erythrocyte membrane protein-1 identifies a CD36 binding domain. Mol Biochem Parasitol 97: 133-148.
44. Smith, J.D., Craig, A.G., Kriek, N., Hudson-Taylor, D., Kyes, S., Fagen, T., et al. (2000a) Identification of a Plasmodium falciparum intercellular adhesion molecule-1 binding domain: a parasite adhesion trait implicated in cerebral malaria. Proc Natl Acad Sci USA 97: 1766-1771.
45. Smith, J.D., Subramanian, G., Gamain, B., Baruch, D.I., and Miller, L.H. (2000b) Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol 110: 293-310.
46. Srivastava, A., Gangnard, S., Round, A., Dechavanne, S., Juillerat, A., Raynal, B., et al. (2010) Full-length extracellular region of the var2CSA variant of PfEMP1 is required for specific, high-affinity binding to CSA. Proc Natl Acad Sci USA 107: 4884-4889.
47. Su, X.Z., Heatwole, V.M., Wertheimer, S.P., Guinet, F., Herrfeldt, J.A., Peterson, D.S., et al. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89-100.
48. Tamez, P.A., Bhattacharjee, S., Van Ooij, C., Hiller, N.L., Llinas, M., Balu, B., et al. (2008) An erythrocyte vesicle protein exported by the malaria parasite promotes tubovesicular lipid import from the host cell surface. PLoS Pathog 4: e1000118.
49. Taylor, K.A., Schmitz, H., Reedy, M.C., Goldman, Y.E., Franzini-Armstrong, C., Sasaki, H., et al. (1999) Tomographic 3D reconstruction of quick-frozen, Ca2+-activated contracting insect flight muscle. Cell 99: 421-431.
50. Templeton, T.J., and Deitsch, K.W. (2005) Targeting malaria parasite proteins to the erythrocyte. Trends Parasitol 21: 399-402.
51. Tokuyasu, K.T. (1973) A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57: 551-565.
52. Tonkin, C.J., Carret, C.K., Duraisingh, M.T., Voss, T.S., Ralph, S.A., Hommel, M., et al. (2009) Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 7: e84.
53. Trager, W., and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
54. Trelka, D.P., Schneider, T.G., Reeder, J.C., and Taraschi, T.F. (2000) Evidence for vesicle-mediated trafficking of parasite proteins to the host cell cytosol and erythrocyte surface membrane in Plasmodium falciparum infected erythrocytes. Mol Biochem Parasitol 106: 131-145.
55. Viebig, N.K., Gamain, B., Scheidig, C., Lepolard, C., Przyborski, J., Lanzer, M., et al. (2005) A single member of the Plasmodium falciparum var multigene family determines cytoadhesion to the placental receptor chondroitin sulphate A. EMBO Rep 6: 775-781.
56. Waller, K.L., Cooke, B.M., Nunomura, W., Mohandas, N., and Coppel, R.L. (1999) Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P. falciparum erythrocyte membrane protein 1 (PfEMP1). J Biol Chem 274: 23808-23813.
57. Waller, K.L., Nunomura, W., Cooke, B.M., Mohandas, N., and Coppel, R.L. (2002) Mapping the domains of the cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) that bind to the knob-associated histidine-rich protein (KAHRP). Mol Biochem Parasitol 119: 125-129.
58. Waterkeyn, J.G., Cowman, A.F., and Cooke, B.M. (2001) Plasmodium falciparum: gelatin enrichment selects for parasites with full-length chromosome 2. implications for cytoadhesion assays. Exp Parasitol 97: 115-118.
59. Wickert, H., Wissing, F., Andrews, K.T., Stich, A., Krohne, G., and Lanzer, M. (2003) Evidence for trafficking of PfEMP1 to the surface of P. falciparum-infected erythrocytes via a complex membrane network. Eur J Cell Biol 82: 271-284.
60. Wickham, M.E., Rug, M., Ralph, S.A., Klonis, N., McFadden, G.I., Tilley, L., and Cowman, A.F. (2001) Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J 20: 5636-5649.