Functional analysis of Plasmodium vivax VIR proteins reveals different subcellular localizations and cytoadherence to the ICAM-1 endothelial receptor

Cellular Microbiology

Volumn 14, Issue 3, 2012, Pages 386-400

  Bernabeu, M ^a   Lopez, F J ^a   Ferrer, M ^a   Martin Jaular, L ^a   Razaname, A ^b   Corradin, G ^b   Maier, A G ^c   del Portillo, H A ^a,d   Fernandez Becerra, C ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c LA TROBE UNIVERSITY   (Australia)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANTIGENIC VARIATION; ARTICLE; CELL ADHESION; CELL COMPARTMENTALIZATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHO CELL; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; MEROZOITE; MULTIGENE FAMILY; NONHUMAN; PARASITE; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION;

CELL MEMBRANE; CULTURE TECHNIQUES; ENDOTHELIAL CELLS; ERYTHROCYTES; GENES, PROTOZOAN; HOST-PARASITE INTERACTIONS; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MEROZOITES; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SCHIZONTS;

PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; VIR;

EID: 84857444327     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01726.x     Document Type: Article

References (47)

1. Ansari, F.A., Kumar, N., Bala Subramanyam, M., Gnanamani, M., and Ramachandran, S. (2008) MAAP: malarial adhesins and adhesin-like proteins predictor. Proteins 70: 659-666.
2. Anstey, N.M., Russell, B., Yeo, T.W., and Price, R.N. (2009) The pathophysiology of vivax malaria. Trends Parasitol 25: 220-227.
3. Atherton, E., and Sheppard, R.C. (1989) Solid Phase Peptide Synthesis: A Practical Approach. Oxford: IRL.
4. Auliff, A.M., Adams, J.H., O'Neil, M.T., and Cheng, Q. (2010) Defining the role of mutations in Plasmodium vivax dihydrofolate reductase-thymidylate synthase gene using an episomal Plasmodium falciparum transfection system. Antimicrob Agents Chemother 54: 3927-3932.
5. Azevedo, M.F., and del Portillo, H.A. (2007) Promoter regions of Plasmodium vivax are poorly or not recognized by Plasmodium falciparum. Malar J 6: 20.
6. Blisnick, T., Morales Betoulle, M.E., Barale, J.C., Uzureau, P., Berry, L., Desroses, S., etal. (2000) Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol Biochem Parasitol 111: 107-121.
7. Bozdech, Z., Mok, S., Hu, G., Imwong, M., Jaidee, A., Russell, B., etal. (2008) The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc Natl Acad Sci USA 105: 16290-16295.
8. Buffet, P.A., Gamain, B., Scheidig, C., Baruch, D., Smith, J.D., Hernandez-Rivas, R., etal. (1999) Plasmodium falciparum domain mediating adhesion to chondroitin sulfate A: a receptor for human placental infection. Proc Natl Acad Sci USA 96: 12743-12748.
9. Carlton, J.M., Adams, J.H., Silva, J.C., Bidwell, S.L., Lorenzi, H., Caler, E., etal. (2008) Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455: 757-763.
10. Carvalho, B.O., Lopes, S.C., Nogueira, P.A., Orlandi, P.P., Bargieri, D.Y., Blanco, Y.C., etal. (2010) On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis 202: 638-647.
11. Cooke, B.M., and Coppel, R.L. (1995) Cytoadhesion and falciparum malaria: going with the flow. Parasitol Today 11: 282-287.
12. Cooke, B.M., Buckingham, D.W., Glenister, F.K., Fernandez, K.M., Bannister, L.H., Marti, M., etal. (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.
13. Corradin, G., Kajava, A.V., and Verdini, A. (2010) Long synthetic peptides for the production of vaccines and drugs: a technological platform coming of age. Sci Transl Med 2: 50rv53.
14. Crabb, B.S., Rug, M., Gilberger, T.W., Thompson, J.K., Triglia, T., Maier, A.G., and Cowman, A.F. (2004) Transfection of the human malaria parasite Plasmodium falciparum. Methods Mol Biol 270: 263-276.
15. D'Ombrain, M.C., Voss, T.S., Maier, A.G., Pearce, J.A., Hansen, D.S., Cowman, A.F., and Schofield, L. (2007) Plasmodium falciparum erythrocyte membrane protein-1 specifically suppresses early production of host interferon-gamma. Cell Host Microbe 2: 130-138.
16. Deitsch, K., Driskill, C., and Wellems, T. (2001) Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 29: 850-853.
17. Fernandez, P., Petres, S., Mecheri, S., Gysin, J., and Scherf, A. (2010) Strain-transcendent immune response to recombinant Var2CSA DBL5-epsilon domain block P. falciparum adhesion to placenta-derived BeWo cells under flow conditions. PLoS ONE 5: e12558.
18. Fernandez-Becerra, C., Pein, O., de Oliveira, T.R., Yamamoto, M.M., Cassola, A.C., Rocha, C., etal. (2005) Variant proteins of Plasmodium vivax are not clonally expressed in natural infections. Mol Microbiol 58: 648-658.
19. Foth, B.J., Ralph, S.A., Tonkin, C.J., Struck, N.S., Fraunholz, M., Roos, D.S., etal. (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708.
20. Golnitz, U., Albrecht, L., and Wunderlich, G. (2008) Var transcription profiling of Plasmodium falciparum 3D7: assignment of cytoadherent phenotypes to dominant transcripts. Malar J 7: 14.
21. Guerra, C.A., Howes, R.E., Patil, A.P., Gething, P.W., Van Boeckel, T.P., Temperley, W.H., etal. (2010) The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS Negl Trop Dis 4: e774.
22. Hay, S.I., Guerra, C.A., Tatem, A.J., Noor, A.M., and Snow, R.W. (2004) The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 4: 327-336.
23. 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.
24. Joergensen, L., Bengtsson, D.C., Bengtsson, A., Ronander, E., Berger, S.S., Turner, L., etal. (2010) Surface co-expression of two different PfEMP1 antigens on single Plasmodium falciparum-infected erythrocytes facilitates binding to ICAM1 and PECAM1. PLoS Pathog 6: e1001083.
25. 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.
26. Kochar, D.K., Saxena, V., Singh, N., Kochar, S.K., Kumar, S.V., and Das, A. (2005) Plasmodium vivax malaria. Emerg Infect Dis 11: 132-134.
27. Kochar, D.K., Tanwar, G.S., Khatri, P.C., Kochar, S.K., Sengar, G.S., Gupta, A., etal. (2010) Clinical features of children hospitalized with malaria - a study from Bikaner, northwest India. Am J Trop Med Hyg 83: 981-989.
28. Kulzer, S., Rug, M., Brinkmann, K., Cannon, P., Cowman, A., Lingelbach, K., etal. (2010) Parasite-encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum-infected erythrocyte. Cell Microbiol 12: 1398-1420.
29. 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.
30. Marsh, K., Marsh, V.M., Brown, J., Whittle, H.C., and Greenwood, B.M. (1988) Plasmodium falciparum: the behavior of clinical isolates in an in vitro model of infected red blood cell sequestration. Exp Parasitol 65: 202-208.
31. 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.
32. Mendis, K., Sina, B.J., Marchesini, P., and Carter, R. (2001) The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64: 97-106.
33. Merino, E.F., Fernandez-Becerra, C., Durham, A.M., Ferreira, J.E., Tumilasci, V.T., d'Arc-Neves, J., etal. (2006) Multi-character population study of the vir subtelomeric multigene superfamily of Plasmodium vivax, a major human malaria parasite. Mol Biochem Parasitol 149: 10-16.
34. Mphande, F.A., Ribacke, U., Kaneko, O., Kironde, F., Winter, G., and Wahlgren, M. (2008) SURFIN4.1, a schizont-merozoite associated protein in the SURFIN family of Plasmodium falciparum. Malar J 7: 116.
35. Mueller, I., Galinski, M.R., Baird, J.K., Carlton, J.M., Kochar, D.K., Alonso, P.L., and Portillo, H.A. (2009) Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 9: 555-566.
36. O'Neil, M.T., Korsinczky, M.L., Gresty, K.J., Auliff, A., and Cheng, Q. (2007) A novel Plasmodium falciparum expression system for assessing antifolate resistance caused by mutant P. vivax dihydrofolate reductase-thymidylate synthase. J Infect Dis 196: 467-474.
37. del Portillo, H.A., Fernandez-Becerra, C., Bowman, S., Oliver, K., Preuss, M., Sanchez, C.P., etal. (2001) A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 410: 839-842.
38. del Portillo, H.A., Lanzer, M., Rodriguez-Malaga, S., Zavala, F., and Fernandez-Becerra, C. (2004) Variant genes and the spleen in Plasmodium vivax malaria. Int J Parasitol 34: 1547-1554.
39. Rug, M., Wickham, M.E., Foley, M., Cowman, A.F., and Tilley, L. (2004) Correct promoter control is needed for trafficking of the ring-infected erythrocyte surface antigen to the host cytosol in transfected malaria parasites. Infect Immun 72: 6095-6105.
40. Sa, J.M., Yamamoto, M.M., Fernandez-Becerra, C., de Azevedo, M.F., Papakrivos, J., Naude, B., etal. (2006) Expression and function of pvcrt-o, a Plasmodium vivax ortholog of pfcrt, in Plasmodium falciparum and Dictyostelium discoideum. Mol Biochem Parasitol 150: 219-228.
41. Salanti, A., Staalsoe, T., Lavstsen, T., Jensen, A.T., Sowa, M.P., Arnot, D.E., etal. (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancyassociated malaria. Mol Microbiol 49: 179-191.
42. Sam-Yellowe, T.Y., Florens, L., Johnson, J.R., Wang, T., Drazba, J.A., Le Roch, K.G., etal. (2004) A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res 14: 1052-1059.
43. Sargeant, T.J., Marti, M., Caler, E., Carlton, J.M., Simpson, K., Speed, T.P., and Cowman, A.F. (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7: R12.
44. Spielmann, T., and Gilberger, T.W. (2010) Protein export in malaria parasites: do multiple export motifs add up to multiple export pathways? Trends Parasitol 26: 6-10.
45. Tonkin, C.J., van Dooren, G.G., Spurck, T.P., Struck, N.S., Good, R.T., Handman, E., etal. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21.
46. Trager, W., and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
47. Winter, G., Kawai, S., Haeggstrom, M., Kaneko, O., von Euler, A., Kawazu, S., etal. (2005) SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med 201: 1853-1863.