PEXEL-independent trafficking of Plasmodium falciparum SURFIN 4.2 to the parasite-infected red blood cell and Maurer's clefts

Parasitology International

Volumn 60, Issue 3, 2011, Pages 313-320

  Alexandre, Jean Semé Fils ^a,b   Yahata, Kazuhide ^a   Kawai, Satoru ^c   Torii, Motomi ^d   Kaneko, Osamu ^a  

^a NAGASAKI UNIVERSITY   (Japan)

^b Centro Nacional de Control de Enfermedades Tropicales   (Dominican Republic)

^c DOKKYO MEDICAL UNIVERSITY   (Japan)

^d EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Malaria; Maurer's clefts; Plasmodium falciparum; Protein trafficking; SURFIN

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEIN SURFIN 4.2; PROTOZOAL PROTEIN; TRITON X 100; UNCLASSIFIED DRUG;

ARTICLE; ERYTHROCYTE; HUMAN; HUMAN CELL; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; WESTERN BLOTTING;

ANIMALS; ANTIGENS, PROTOZOAN; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GREEN FLUORESCENT PROTEINS; HOST-PARASITE INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; MALARIA, FALCIPARUM; MEMBRANE PROTEINS; ORGANISMS, GENETICALLY MODIFIED; PLASMODIUM FALCIPARUM; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS;

PLASMODIUM FALCIPARUM;

EID: 79959506789     PISSN: 13835769     EISSN: 18730329     Source Type: Journal    
DOI: 10.1016/j.parint.2011.05.003     Document Type: Article

References (37)

1. Tilley L., Sougrat R., Lithgow T., Hanssen E. The twists and turns of Maurer's cleft trafficking in P. falciparum-infected erythrocytes. Traffic 2008, 9:187-197.
2. Przyborski J.M., Wickert H., Krohne G., Lanzer M. Maurer's clefts - a novel secretory organelle?. Mol Biochem Parasitol 2003, 132:17-26.
3. Lanzer M., Wickert H., Krohne G., Vincensini L., Braun-Breton C. Maurer's clefts: a novel multi-functional organelle in the cytoplasm of Plasmodium falciparum-infected erythrocytes. Int J Parasitol 2006, 36:23-36.
4. Wickham M.E., Rug M., Ralph S.A., Klonis N., McFadden G.I., Tilley L., et al. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J 2001, 20:5636-5649.
5. Baruch D.I. Adhesive receptors on malaria-parasitized red cells. Baillière's Best Pract Res Clin Haematol 1999, 12:747-761.
6. Chen Q., Schlichtherle M., Wahlgren M. Molecular aspects of severe malaria. Clin Microbiol Rev 2000, 13:439-450.
7. Newbold C., Craig A., Kyes S., Rowe A., Fernandez-Reyes D., Fagan T. Cytoadherence, pathogenesis and the infected red cell surface in Plasmodium falciparum. Int J Parasitol 1999, 29:927-937.
8. Hiller N.L., Bhattacharjee S., van Ooij C., Liolios K., Harrison T., Lopez-Estraño C., et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004, 306:1934-1937.
9. Marti M., Good R.T., Rug M., Knuepfer E., Cowman A.F. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 2004, 306:1930-1933.
10. Marti M., Baum J., Rug M., Tilley L., Cowman A.F. Signal-mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol 2005, 171:587-592.
11. Saridaki T., Fröhlich K.S., Braun-Breton C., Lanzer M. Export of PfSBP1 to the Plasmodium falciparum Maurer's clefts. Traffic 2009, 10:137-152.
12. Boddey J.A., Hodder A.N., Günther S., Gilson P.R., Patsiouras H., Kapp E.A., et al. An aspartyl protease directs malaria effector proteins to the host cell. Nature 2010, 463:627-631.
13. Russo I., Babbitt S., Muralidharan V., Butler T., Oksman A., Goldberg D.E. Plasmepsin V licenses Plasmodium proteins for export into the host erythrocyte. Nature 2010, 463:632-636.
14. de Koning-Ward T.F., Gilson P.R., Boddey J.A., Rug M., Smith B.J., Papenfuss A.T., et al. A newly discovered protein export machine in malaria parasites. Nature 2009, 459:945-949.
15. Melcher M., Muhle R.A., Henrich P.P., Kraemer S.M., Avril M., Vigan-Womas I., et al. Identification of a role for the PfEMP1 semi-conserved head structure in protein trafficking to the surface of Plasmodium falciparum infected red blood cells. Cell Microbiol 2010, 12:1446-1462.
16. van Ooij C., Tamez P., Bhattacharjee S., Hiller N.L., Harrison T., Liolios K., et al. The malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathog 2008, 4:e1000084.
17. Spielmann T., Hawthorne P.L., Dixon M.W., Hannemann M., Klotz K., Kemp D.J., et al. A cluster of ring stage-specific genes linked to a locus implicated in cytoadherence in Plasmodium falciparum codes for PEXEL-negative and PEXEL-positive proteins exported into the host cell. Mol Biol Cell 2006, 17:3613-3624.
18. Blisnick T., Morales Betoulle M.E., Barale J.C., Uzureau P., Berry L., Desroses S., et al. Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol Biochem Parasitol 2000, 111:107-121.
19. Spycher C., Klonis N., Spielmann T., Kump E., Steiger S., Tilley L., et al. MAHRP-1, a novel Plasmodium falciparum histidine-rich protein, binds ferriprotoporphyrin IX and localizes to the Maurer's clefts. J Biol Chem 2003, 278:35373-35383.
20. Hawthorne P.L., Trenholme K.R., Skinner-Adams T.S., Spielmann T., Fischer K., Dixon M.W., et al. A novel Plasmodium falciparum ring stage protein, REX, is located in Maurer's clefts. Mol Biochem Parasitol 2004, 136:181-189.
21. Hanssen E., Hawthorne P., Dixon M.W., Trenholme K.R., McMillan P.J., Spielmann T., et al. Targeted mutagenesis of the ring-exported protein-1 of Plasmodium falciparum disrupts the architecture of Maurer's cleft organelles. Mol Microbiol 2008, 69:938-953.
22. Saridaki T., Sánchez C.P., Pfahler J., Lanzer M. A conditional export system provides new insights into protein export in Plasmodium falciparum-infected erythrocytes. Cell Microbiol 2008, 10:2483-2495.
23. Spielmann T., Gilberger T.W. Protein export in malaria parasites: do multiple export motifs add up to multiple export pathways?. Trends Parasitol 2009, 26:6-10.
24. Haase S., Herrmann S., Grüring C., Heiber A., Jansen P.W., Langer C., et al. Sequence requirements for the export of the Plasmodium falciparum Maurer's clefts protein REX2. Mol Microbiol 2009, 71:1003-1017.
25. Dixon M.W., Hawthorne P.L., Spielmann T., Anderson K.L., Trenholme K.R., Gardiner D.L. Targeting of the ring exported protein 1 to the Maurer's clefts is mediated by a two-phase process. Traffic 2008, 9:1316-1326.
26. Winter G., Kawai S., Haeggström M., Kaneko O., von Euler A., Kawazu S., et al. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med 2005, 201:1853-1863.
27. van Dooren G.G., Marti M., Tonkin C.J., Stimmler L.M., Cowman A.F., McFadden G.I. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol 2005, 57:405-419.
28. Le Roch K.G., Zhou Y., Blair P.L., Grainger M., Moch J.K., Haynes J.D., et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 2003, 301:1503-1508.
29. Aurrecoechea C., Brestelli J., Brunk B.P., Dommer J., Fischer S., Gajria B., et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 2009, 37:D539-D543.
30. Nakazawa S., Culleton R., Maeno Y. In vivo and in vitro gametocyte production of Plasmodium falciparum isolates from Northern Thailand. Int J Parasitol 2011, 41:317-323.
31. Deitsch K., Driskill C., Wellems T. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 2001, 29:850-853.
32. Tonkin C.J., van Dooren G.G., Spurck T.P., Struck N.S., Good R.T., Handman E., et al. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 2004, 137:13-21.
33. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
34. Marshall V.M., Coppel R.L. Characterisation of the gene encoding adenylosuccinate lyase of Plasmodium falciparum. Mol Biochem Parasitol 1997, 88:237-241.
35. Aley S.B., Sherwood J.A., Howard R.J. Knob-positive and knob-negative Plasmodium falciparum differ in expression of a strain-specific malarial antigen on the surface of infected erythrocytes. J Exp Med 1984, 160:1585-1590.
36. Oh S.S., Voigt S., Fisher D., Yi S.J., LeRoy P.J., Derick L.H., et al. 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 2000, 108:237-247.
37. Waller K.L., Stubberfield L.M., Dubljevic V., Buckingham D.W., Mohandas N., Coppel R.L., et al. Interaction of the exported malaria protein Pf332 with the red blood cell membrane skeleton. Biochim Biophys Acta 2010, 1798:861-871.