The N-terminal segment of Plasmodium falciparum SURFIN4.1 is required for its trafficking to the red blood cell cytosol through the endoplasmic reticulum

Parasitology International

Volumn 62, Issue 2, 2013, Pages 215-229

  Zhu, Xiaotong ^a   Yahata, Kazuhide ^a   Alexandre, Jean Semé Fils ^a,b   Tsuboi, Takafumi ^c   Kaneko, Osamu ^a  

^a NAGASAKI UNIVERSITY   (Japan)

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

^c EHIME UNIVERSITY   (Japan)

Author keywords

Malaria; Plasmodium falciparum; Red blood cell; Signal; Trafficking

Indexed keywords

BREFELDIN A; MEMBRANE PROTEIN; SURFIN 4.1 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ERYTHROCYTE; EXON; INTRON; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; BREFELDIN A; CYTOSOL; ENDOPLASMIC RETICULUM; ERYTHROCYTES; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; PLASMODIUM FALCIPARUM; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; TRYPTOPHAN;

PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX;

EID: 84873733356     PISSN: 13835769     EISSN: 18730329     Source Type: Journal    
DOI: 10.1016/j.parint.2012.12.006     Document Type: Article

References (65)

1. Richards J.S., Beeson J.G. The future for blood-stage vaccines against malaria. Immunology and Cell Biology 2009, 87:377-390.
2. World Health Organization World Malaria Report 2011 2011, World Health Organization, Geneva, Switzerland.
3. Miller L.H., Baruch D.I., Marsh K., Doumbo O.K. The pathogenic basis of malaria. Nature 2002, 415:673-679.
4. Kirk K. Membrane transport in the malaria-infected erythrocyte. Physiological Reviews 2001, 81:495-537.
5. Fischer K., Marti T., Rick B., Johnson D., Benting J., Baumeister S., et al. Characterization and cloning of the gene encoding the vacuolar membrane protein EXP-2 from Plasmodium falciparum. Molecular and Biochemical Parasitology 1998, 92:47-57.
6. Langreth S.G., Jensen J.B., Reese R.T., Trager W. Fine structure of human malaria in vitro. The Journal of Protozoology 1978, 25:443-452.
7. 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. Molecular Microbiology 2008, 69:938-953.
8. 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. Molecular Biology of the Cell 2006, 17:3613-3624.
9. Spycher C., Rug M., Klonis N., Ferguson D.J., Cowman A.F., Beck H.P., et al. Genesis of and trafficking to the Maurer's clefts of Plasmodium falciparum-infected erythrocytes. Molecular and Cellular Biology 2006, 26:4074-4085.
10. Barnwell J.W. Vesicle-mediated transport of membrane and proteins in malaria-infected erythrocytes. Blood Cells 1990, 16:379-395.
11. Hinterberg K., Scherf A., Gysin J., Toyoshima T., Aikawa M., Mazie J.C., et al. Plasmodium falciparum: the Pf332 antigen is secreted from the parasite by a brefeldin A-dependent pathway and is translocated to the erythrocyte membrane via the Maurer's clefts. Experimental Parasitology 1994, 79:279-291.
12. Przyborski J.M., Wickert H., Krohne G., Lanzer M. Maurer's clefts - a novel secretory organelle?. Molecular and Biochemical Parasitology 2003, 132:17-26.
13. 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.
14. Knuepfer E., Rug M., Klonis N., Tilley L., Cowman A.F. Trafficking of the major virulence factor to the surface of transfected P. falciparum-infected erythrocytes. Blood 2005, 105:4078-4087.
15. Templeton T.J., Deitsch K.W. Targeting malaria parasite proteins to the erythrocyte. Trends in Parasitology 2005, 21:399-402.
16. Su X.Z., Heatwole V.M., Wertheimer S.P., Guinet F., Herrfeldt J.A., Peterson D.S., et al. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 1995, 82:89-100.
17. Crabb B.S., Cooke B.M., Reeder J.C., Waller R.F., Caruana S.R., Davern K.M., et al. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 1997, 89:287-296.
18. Waller K.L., Cooke B.M., Nunomura W., Mohandas N., Coppel R.L. 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). The Journal of Biological Chemistry 1999, 274:23808-23813.
19. Kyes S.A., Rowe J.A., Kriek N., Newbold C.I. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:9333-9338.
20. Fernandez V., Hommel M., Chen Q., Hagblom P., Wahlgren M. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. The Journal of Experimental Medicine 1999, 190:1393-1404.
21. Haeggström M., von Euler A., Kironde F., Fernandez V., Wahlgren M. Characterization of Maurer's clefts in Plasmodium falciparum-infected erythrocytes. The American Journal of Tropical Medicine and Hygiene 2007, 76:27-32.
22. Kaviratne M., Khan S.M., Jarra W., Preiser P.R. Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryotic Cell 2002, 1:926-935.
23. Przyborski J.M., Miller S.K., Pfahler J.M., Henrich P.P., Rohrbach P., Crabb B.S., et al. Trafficking of STEVOR to the Maurer's clefts in Plasmodium falciparum-infected erythrocytes. The EMBO Journal 2005, 24:2306-2317.
24. 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. Molecular and Biochemical Parasitology 2000, 111:107-121.
25. 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. Molecular and Biochemical Parasitology 2004, 136:181-189.
26. Pachlatko E., Rusch S., Muller A., Hemphill A., Tilley L., Hanssen E., et al. MAHRP2, an exported protein of Plasmodium falciparum, is an essential component of Maurer's cleft tethers. Molecular Microbiology 2010, 77:1136-1152.
27. 4.2 to the parasite-infected red blood cell and Maurer's clefts. Parasitology International 2011, 60:313-320.
28. Cooke B.M., Buckingham D.W., Glenister F.K., Fernandez K.M., Bannister L.H., Marti M., et al. A Maurer's cleft-associated protein is essential for expression of the major malaria virulence antigen on the surface of infected red blood cells. The Journal of Cell Biology 2006, 172:899-908.
29. Maier A.G., Rug M., O'Neill M.T., Beeson J.G., Marti M., Reeder J., et al. Skeleton-binding protein 1 functions at the parasitophorous vacuole membrane to traffic PfEMP1 to the Plasmodium falciparum-infected erythrocyte surface. Blood 2007, 109:1289-1297.
30. Haldar K. Intracellular trafficking in Plasmodium-infected erythrocytes. Current Opinion in Microbiology 1998, 1:466-471.
31. Lingelbach K. Protein trafficking in the Plasmodium-falciparum infected erythrocyte=from models to mechanisms. Annals of Tropical Medicine and Parasitology 1997, 91:543-549.
32. Hiller N.L., Bhattacharjee S., van Ooij C., Liolios K., Harrison T., Lopez-Estrano C., et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004, 306:1934-1937.
33. 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.
34. 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. The Journal of Biological Chemistry 2003, 278:35373-35383.
35. Spielmann T., Gilberger T.W. Protein export in malaria parasites: do multiple export motifs add up to multiple export pathways?. Trends in Parasitology 2010, 26:6-10.
36. 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. The Journal of Experimental Medicine 2005, 201:1853-1863.
37. 4.1, a schizont-merozoite associated protein in the SURFIN family of Plasmodium falciparum. Malaria Journal 2008, 7:116.
38. 4.2 in Plasmodium falciparum isolates from Thailand. Parasitology International 2012, 61:317-323.
39. Fonager J., Cunningham D., Jarra W., Koernig S., Henneman A.A., Langhorne J., et al. Transcription and alternative splicing in the yir multigene family of the malaria parasite Plasmodium y. yoelii: identification of motifs suggesting epigenetic and post-transcriptional control of RNA expression. Molecular and Biochemical Parasitology 2007, 156:1-11.
40. Carlton J.M., Adams J.H., Silva J.C., Bidwell S.L., Lorenzi H., Caler E., et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008, 455:757-763.
41. Fernandez-Becerra C., Yamamoto M.M., Vencio R.Z., Lacerda M., Rosanas-Urgell A., del Portillo H.A. Plasmodium vivax and the importance of the subtelomeric multigene vir superfamily. Trends in Parasitology 2009, 25:44-51.
42. 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 Pathogens 2008, 4:e1000084.
43. Sargeant T.J., Marti M., Caler E., Carlton J.M., Simpson K., Speed T.P., et al. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biology 2006, 7:R12.
44. Walliker D., Quakyi I.A., Wellems T.E., McCutchan T.F., Szarfman A., London W.T., et al. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 1987, 236:1661-1666.
45. Kaneko O., Soubes S.C., Miller L.H. Plasmodium falciparum: invasion of Aotus monkey red blood cells and adaptation to Aotus monkeys. Experimental Parasitology 1999, 93:116-119.
46. Nakazawa S., Culleton R., Maeno Y. In vivo and in vitro gametocyte production of Plasmodium falciparum isolates from Northern Thailand. International Journal for Parasitology 2011, 41:317-323.
47. Trager W., Jenson J.B. Cultivation of malarial parasites. Nature 1978, 273:621-622.
48. Lambros C., Vanderberg J.P. Synchronization of Plasmodium falciparum erythrocytic stages in culture. The Journal of Parasitology 1979, 65:418-420.
49. Deitsch K., Driskill C., Wellems T. Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Research 2001, 29:850-853.
50. 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. The EMBO Journal 2001, 20:5636-5649.
51. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 2001, 305:567-580.
52. 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. Molecular Microbiology 2005, 57:405-419.
53. Noe A.R., Fishkind D.J., Adams J.H. Spatial and temporal dynamics of the secretory pathway during differentiation of the Plasmodium yoelii schizont. Molecular and Biochemical Parasitology 2000, 108:169-185.
54. Bozdech Z., Zhu J., Joachimiak M.P., Cohen F.E., Pulliam B., DeRisi J.L. Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biology 2003, 4:R9.
55. Grüring C., Heiber A., Kruse F., Ungefehr J., Gilberger T.W., Spielmann T. Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions. Nature Communications 2011, 2:165.
56. Saridaki T., Frohlich K.S., Braun-Breton C., Lanzer M. Export of PfSBP1 to the Plasmodium falciparum Maurer's clefts. Traffic 2009, 10:137-152.
57. 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. Molecular Microbiology 2009, 71:1003-1017.
58. Boyd D., Beckwith J. Positively charged amino acid residues can act as topogenic determinants in membrane proteins. Proceedings of the National Academy of Sciences of the United States of America 1989, 86:9446-9450.
59. von Heijne G. Principles of membrane protein assembly and structure. Progress in Biophysics and Molecular Biology 1996, 66:113-139.
60. Bogdanov M., Xie J., Dowhan W. Lipid-protein interactions drive membrane protein topogenesis in accordance with the positive inside rule. The Journal of Biological Chemistry 2009, 284:9637-9641.
61. 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.
62. Crabb B.S., de Koning-Ward T.F., Gilson P.R. Protein export in Plasmodium parasites: from the endoplasmic reticulum to the vacuolar export machine. International Journal for Parasitology 2010, 40:509-513.
63. Boddey J.A., Hodder A.N., Gunther 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.
64. Bhattacharjee S., Stahelin R.V., Speicher K.D., Speicher D.W., Haldar K. Endoplasmic reticulum PI(3)P lipid binding targets malaria proteins to the host cell. Cell 2012, 148:201-212.
65. Grüring C., Heiber A., Kruse F., Flemming S., Franci G., Colombo S.F., et al. Uncovering common principles in protein export of malaria parasites. Cell Host & Microbe 2012, 12:717-729.