Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte

Traffic

Volumn 10, Issue 3, 2009, Pages 285-299

  Boddey, Justin A ^a   Moritz, Robert L ^a   Simpson, Richard J ^a   Cowman, Alan F ^a  

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

Author keywords

Acetylation; Malaria; PEXEL; Signal sequence; Trafficking

Indexed keywords

ARGININE; LEUCINE; PLASMODIUM EXPORT ELEMENT; PROTEINASE; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ERYTHROCYTE; HOST CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PARASITE SURVIVAL; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TRANSPORT; TRANSGENIC ORGANISM;

ACETYLATION; ANIMALS; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ERYTHROCYTES; HUMANS; MASS SPECTROMETRY; PLASMODIUM FALCIPARUM; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

EID: 59849124093     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00864.x     Document Type: Article

References (49)

1. Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 2005;434:214-217.
2. Marti M, Baum J, Rug M, Tilley L, Cowman AF. Signal-mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol 2005;171:587-592.
3. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 1995;82:101-110.
4. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Taraschi TF, Howard RJ. Cloning the P.falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 1995;82:77-87.
5. Su X-Z, Kirkman LA, Fujioka H, Wellems TE. Complex polymorphisms in an ∼330 kDa protein are linked to chloroquine-resistant P. falciparum in Southeast Asia and Africa. Cell 1997;91:593-603.
6. Kraemer SM, Smith JD. A family affair: Var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 2006;9:374-380.
7. Wickham ME, Rug M, Ralph SA, Klonis N, McFadden GI, Tilley L, Cowman AF. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum -infected human erythrocytes. EMBO J 2001;20:1-14.
8. Lopez-Estrano C, Bhattacharjee S, Harrison T, Haldar K. Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum -infected erythrocytes. Proc Natl Acad Sci USA 2003;100:12402-12407.
9. Kriek N, Tilley L, Horrocks P, Pinches R, Elford BC, Ferguson DJ, Lingelbach K, Newbold CI. Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Mol Microbiol 2003;50:1215-1227.
10. Papakrivos J, Newbold CI, Lingelbach K. A potential novel mechanism for the insertion of a membrane protein revealed by a biochemical analysis of the Plasmodium falciparum cytoadherence molecule PfEMP-1. Mol Microbiol 2005;55:1272-1284.
11. Knuepfer E, Rug M, Klonis N, Tilley L, Cowman AF. Trafficking of the major virulence factor to the surface of transfected P. falciparum -infected erythrocytes. Blood 2005;105: 4078-4087.
12. Cooke BM, Buckingham DW, Glenister FK, Fernandez KM, Bannister LH, Marti M, Mohandas N, Coppel RL. 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 2006;172:899-908.
13. Maier AG, Rug M, O'Neill MT, Beeson JG, Marti M, Reeder J, Cowman AF. 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.
14. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, Szestak T, Chesson J, Wu Y, Hughes K, Coppel RL, Newbold C, Beeson JG, Craig A, Crabb BS, Cowman AF. Exported proteins required for virulence and rigidity of Plasmodium falciparum -infected human erythrocytes. Cell 2008;134:48-61.
15. Spycher C, Rug M, Pachlatko E, Hanssen E, Ferguson D, Cowman AF, Tilley L, Beck HP. The Maurer's cleft protein MAHRP1 is essential for trafficking of PfEMP1 to the surface of Plasmodium falciparum-infected erythrocytes. Mol Microbiol 2008;68:1300-1314.
16. Baumeister S, Winterberg M, Duranton C, Huber SM, Lang F, Kirk K, Lingelbach K. Evidence for the involvement of Plasmodium falciparum proteins in the formation of new permeability pathways in the erythrocyte membrane. Mol Microbiol 2006;60:493-504.
17. Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, Wickham ME, Brown GV, Coppel RL, Cowman AF. Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 1997;89:287-296.
18. Glenister FK, Coppel RL, Cowman AF, Mohandas N, Cooke BM. Contribution of parasite proteins to altered mechanical properties of malaria-infected red blood cells. Blood 2002;99:1060-1063.
19. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 2004;306:1930-1933.
20. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, Haldar K. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004;306:1934-1937.
21. Singh AP, Buscaglia CA, Wang Q, Levay A, Nussenzweig DR, Walker JR, Winzeler EA, Fujii H, Fontoura BM, Nussenzweig V. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 2007;131:492-504.
22. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, Speed TP, Cowman AF. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 2006;7:R12.
23. Ravetch JV, Kochan J, Perkins M. Isolation of the gene for a glycophorin-binding protein implicated in erythrocyte invasion by a malaria parasite. Science 1985;227:1593-1597.
24. Chang HH, Falick AM, Carlton PM, Sedat JW, DeRisi JL, Marletta MA. N-terminal processing of proteins exported by malaria parasites. Mol Biochem Parasitol 2008;160:107-115.
25. Hiller NL, Akompong T, Morrow JS, Holder AA, Haldar K. Identification of a stomatin orthologue in vacuoles induced in human erythrocytes by malaria parasites. A role for microbial raft proteins in apicomplexan vacuole biogenesis. J Biol Chem 2003;278:48413-48421.
26. Fischer K, Marti T, Rick B, Johnson D, Benting J, Baumeister S, Helmbrecht C, Lanzer M, Lingelbach K. Characterization and cloning of the gene encoding the vacuolar membrane protein EXP-2 from Plasmodium falciparum. Mol Biochem Parasitol 1998;92:47-57.
27. La Greca N, Hibbs AR, Riffkin C, Foley M, Tilley L. Identification of an endoplasmic reticulum-resident calcium-binding protein with multiple EF-hand motifs in asexual stages of Plasmodium falciparum. Mol Biochem Parasitol 1997;89:283-293.
28. Wiek S, Cowman AF, Lingelbach K. Double cross-over gene replacement within the sec 7 domain of a GDP-GTP exchange factor from Plasmodium falciparum allows the generation of a transgenic brefeldin A-resistant parasite line. Mol Biochem Parasitol 2004;138:51-55.
29. Lingelbach K, Przyborski JM. The long and winding road: Protein trafficking mechanisms in the Plasmodium falciparum infected erythrocyte. Mol Biochem Parasitol 2006;147:1-8.
30. Waller RF, Reed MB, Cowman AF, McFadden GI. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 2000;19:1794-1802.
31. Przyborski JM, Miller SK, Pfahler JM, Henrich PP, Rohrbach P, Crabb BS, Lanzer M. Trafficking of STEVOR to the Maurer's clefts in Plasmodium falciparum - infected erythrocytes. EMBO J 2005;24:2306-2317.
32. Saridaki T, Sanchez CP, 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.
33. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004;340:783-795.
34. Lippincott-Schwartz J, Roberts TH, Hirschberg K. Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 2000;16:557-589.
35. Sato K, Nakano A. Mechanisms of COPII vesicle formation and protein sorting. FEBS Lett 2007;581:2076-2082.
36. Martinez-Menarguez JA, Geuze HJ, Slot JW, Klumperman J. Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 1999;98:81-90.
37. Albano FR, Berman A, La Greca N, Hibbs AR, Wickham M, Foley M, Tilley L. A homologue of SAR1p localises to a novel trafficking pathway in malaria-infected erythrocytes. Eur J Cell Biol 1999;78:453-462.
38. Wickert H, Wissing F, Andrews KT, Stich A, Krohne G, Lanzer M. Evidence for trafficking of PfEMP1 to the surface of P. falciparum - infected erythrocytes via a complex membrane network. Eur J Cell Biol 2003;82:271-284.
39. Struck NS, Herrmann S, Schmuck-Barkmann I, de Souza Dias S, Haase S, Cabrera AL, Treeck M, Bruns C, Langer C, Cowman AF, Marti M, Spielmann T, Gilberger TW. Spatial dissection of the cis- and trans-Golgi compartments in the malaria parasite Plasmodium falciparum. Mol Microbiol 2008;67:1320-1330.
40. Adisa A, Frankland S, Rug M, Jackson K, Maier AG, Walsh P, Lithgow T, Klonis N, Gilson PR, Cowman AF, Tilley L. Re-assessing the locations of components of the classical vesicle-mediated trafficking machinery in transfected Plasmodium falciparum. Int J Parasitol 2007;37:1127-1141.
41. Lee MC, Moura PA, Miller EA, Fidock DA. Plasmodium falciparum Sec24 marks transitional ER that exports a model cargo via a diacidic motif. Mol Microbiol 2008;68:1535-1546.
42. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002;419:498-511.
43. Adisa A, Rug M, Foley M, Tilley L. Characterisation of a delta-COP homologue in the malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 2002;123:11-21.
44. van Ooij C, Haldar K. Protein export from Plasmodium parasites. Cell Microbiol 2007;9:573-582.
45. Adisa A, Rug M, Klonis N, Foley M, Cowman AF, Tilley L. The signal sequence of exported protein-1 directs the green fluorescent protein to the parasitophorous vacuole of transfected malaria parasites. J Biol Chem 2003;278:6532-6542.
46. Duraisingh MT, Triglia T, Cowman AF. Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int J Parasitol 2002;32:81-89.
47. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 1997;10:1-6.
48. Baum J, Richard D, Healer J, Rug M, Krnajski Z, Gilberger TW, Green JL, Holder AA, Cowman AF. A conserved molecular motor drives cell invasion and gliding motility across malaria life cycle stages and other apicomplexan parasites. J Biol Chem 2006;281: 5197-5208.
49. Ansorge I, Benting J, Bhakdi S, Lingelbach K. Protein sorting in Plasmodium falciparum - infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem J 1996;315:307-314.