Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway

EMBO Journal

Volumn 19, Issue 8, 2000, Pages 1794-1802

  Waller, Ross F ^a   Reed, Michael B ^b   Cowman, Alan F ^b   McFadden, Geoffrey I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

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

Author keywords

Green fluorescent protein; Malaria; Plastid targeting; Secretory pathway; Transfection

Indexed keywords

CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN; SIGNAL PEPTIDE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SECRETION; CHLOROPLAST; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PLASTID; PRIORITY JOURNAL; PROTEIN TARGETING;

ANIMALIA; PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 0034678922     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.8.1794     Document Type: Article

References (51)

1. Bhaya, D. and Grossman, A. (1991) Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol. Gen. Genet., 229, 400-404.
2. Bodyl, A. (1999) How are plastid proteins of the apicomplexan parasites imported? A hypothesis. Acta Protozool., 38, 31-37.
3. Cavalier-Smith, T. (1982) The origins of plastids. Biol. J. Linn. Soc., 17, 289-306.
4. Cline, K. and Henry, R. (1996) Import and routing of nucleus-encoded chloroplast proteins. Annu. Rev. Cell. Dev. Biol., 12, 1-26.
5. Clough, B., Strath, M., Preiser, P., Denny, P. and Wilson, R. (1997) Thiostrepton binds to malarial plastid rRNA. FEBS Lett., 406, 123-125.
6. Clough, B., Rangachari, K., Strath, M., Preiser, P.R. and Wilson, R. (1999) Antibiotic inhibitors of organellar protein synthesis in Plasmodium falciparum. Protist, 150, 189-195.
7. Crabb, B.S., Triglia, T., Waterkeyn, J.G. and Cowman, A.F. (1997) Stable transgene expression in Plasmodium falciparum. Mol. Biochem. Parasitol., 90, 131-144.
8. Delwiche, C. (1999) Tracing the tread of plastid diversity through the tapestry of life. Am. Nat., 154, S164-S177.
9. Emanuelsson, O., Nielsen, H. and von Heijne, G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci., 8, 978-984.
10. Fichera, M.E. and Roos, D.S. (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature, 390, 407-409.
11. 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.
12. Foley, M. and Tilley, L. (1998) Protein trafficking in malaria-infected erythrocytes. Int. J. Parasitol., 28, 1671-1680.
13. Gibbs, S.P. (1979) The route of entry of cytoplasmically synthesized proteins into chloroplasts of algae possessing chloroplast ER. J. Cell Sci., 35, 253-266.
14. Hohenberg, H., Mannweiler, K. and Muller, M. (1994) High-pressure freezing of cell suspensions in cellulose capillary tubes. J. Microsc., 175, 34-43.
15. Hopkins, J., Fowler, R., Krishna, S., Wilson, I., Mitchell, G. and Bannister, L. (1999) The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist, 150, 283-295.
16. Howard, R.F. and Schmidt, C.M. (1995) The secretory pathway of Plasmodium falciparum regulates transport of p82/rap-1 to the rhoptries. Mol. Biochem. Parasitol., 74, 43-54.
17. Jomaa, H. et al. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science, 285, 1573-1576.
18. Keegstra, K. and Cline, K. (1999) Protein import and routing systems of chloroplasts. Plant Cell, 11, 557-570.
19. Keegstra, K. and Olsen, L. (1989) Chloroplastic precursors and their transport across the envelope membranes. Annu. Rev. Plant Physiol. Plant Mol. Biol., 40, 471-501.
20. Keeling, P.J., Palmer, J.D., Donald, R.G.K., Roos, D.S., Waller, R.F. and McFadden, G.I. (1998) Shikimate pathway in apicomplexan parasites. Nature. 397, 219-220.
21. Köhler, S., Delwiche, C.F., Denny, P.W., Tilney, L.G., Webster, P., Wilson, R.J.M., Palmer, J.D. and Roos, D.S. (1997) A plastid of probable green algal origin in apicomplexan parasites. Science, 275, 1485-1488.
22. Kroth, P. and Strotmann, H. (1999) Diatom plastids: secondary endocytobiosis, plastid genome and protein import. Physiol. Plant., 107, 136-141.
23. Kudo, R. (1971) Protozoology. Charles C. Thomas, Springfield, IL.
24. Lang, M., Apt, K.E. and Kroth, P.G. (1998) Protein transport into complex diatom plastids utilizes two different targeting signals. J. Biol. Chem., 273, 30973-30978.
25. Liaud, M.-F., Brandt, U., Scherzinger, M. and Cerff, R. (1997) Evolutionary origin of cryptomonad microalgae: two novel chloroplast/cytosol-specific GAPDH genes as potential markers of ancestral endosymbiont and host cell components. J. Mol. Evol. (Suppl. 1), 44, S28-S37.
26. Martin, W. and Herrmann, R.G. (1998) Gene transfer from organelles to the nucleus: how much, what happens and why? Plant Physiol., 118, 9-17.
27. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M. and Kowallik, K. (1998) Gene transfer to the nucleus and the evolution of chloroplasts. Nature, 393, 162-165.
28. McFadden, G.I. and Gilson, P.R. (1997) What's eating Eu? The role of eukaryote/eukaryote endosymbioses in plastid origins. In Schenk, H.E.A., Herrmann, R., Jeon, K.W., Müller, N.E. and Schwemmler, W. (eds), Eukaryotism and Symbiosis. Springer-Verlag, Heidelberg, Germany, pp. 24-39.
29. McFadden, G.I. and Roos, D.S. (1999) Apicomplexan plastids as drug targets. Trends Microbiol., 6, 328-333.
30. McFadden, G.I. and Waller, R.F. (1997) Plastids in parasites of humans. BioEssays, 19, 1033-1040.
31. McFadden, G.I., Reith, M., Munholland, J. and Lang-Unnasch, N. (1996) Plastid in human parasites. Nature, 381, 482.
32. McFadden, G.I., Waller, R.F., Reith, M., Munholland, J. and Lang-Unnasch, N. (1997) Plastids in apicomplexan parasites. Pl. Syst. Evol. (Suppl.), 11, 261-287.
33. Nakai, K. and Kanehisa, M. (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics, 14, 897-911.
34. Nielsen, H., Engelbrecht, J., Brunak, S. and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng., 10, 1-6.
35. Osafune, T., Schiff, J. and Hase, E. (1991) Stage-dependent localization of LHCP II apoprotein in the Golgi of synchronized cells of Euglena gracilis by immunogold electron microscopy. Exp. Cell Res., 193, 320-330.
36. Palmer, J.D. and Delwiche, C.F. (1998) The origin and evolution of plastids and their genomes. In Soltis, D.E., Soltis, P.S. and Doyle, J.J. (eds), Molecular Systematics of Plants II. Chapman Hall, New York, NY, pp. 375-409.
37. Read, M., Sherwin, T., Holloway, S., Gull, K. and Hyde, J. (1993) Microtubular organization visualized by immunofluorescence microscopy during erythrocytic schizogony in Plasmodium falciparum and investigation of post-translational modifications of parasite tubulin. Parasitology, 106, 223-232.
38. Reed, M.B., Saliba, K.J., Caruana, S.R., Kirk, K. and Cowman, A.F. (2000) Pgh1 modulates sensitivity and resistance to multiple antimalarials in Plasmodium falciparum. Nature, 403, 906-909.
39. Richter, S. and Lamppa, G.K. (1998) A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc. Natl Acad. Sci. USA, 95, 7463-7468.
40. Schwartzbach, S.D., Osafune, T. and Loffelhardt, W. (1998) Protein import into cyanelles and complex chloroplasts. Plant Mol. Biol., 38, 247-263.
41. Speer, C.A. and Dubey, J.P. (1999) Ultrastructure of schizonts and merozoites of Sarcocystis falcatula in the lungs of budgerigars (Melopsittacus undulatus). J. Parasitol., 85, 630-637.
42. Striepen, B., He, C.Y., Matrajt, M., Soldati, D. and Roos, D.S. (1998) Expression, selection and organellar targeting of the green fluorescent protein in Toxoplasma gondii. Mol. Biochem. Parasitol., 92, 328-338.
43. Sulli, C. and Schwartzbach, S.D. (1995) The polyprotein precursor of the Euglena light-harvesting chlorophyll a/b binding protein is transported to the Golgi apparatus prior to chloroplast import and polyprotein processing. J. Biol. Chem., 270, 13084-13090.
44. Sulli, C., Fang, Z.W., Muchal, U. and Schwartzbach, S.D. (1999) Topology of Euglena chloroplast protein precursors within the endoplasmic reticulum to Golgi to chloroplast transport vesicles. J. Biol. Chem., 274, 457-463.
45. Trager, W. and Jensen, J. (1976) Human malaria parasites in continuous culture. Science, 193, 673-675.
46. Triglia, T., Wang, P., Sims, P.F.G., Hyde, J.E. and Cowman, A.F. (1998) Allelic exchange at the endogenous genomic locus in Plasmodium falciparum proves the role of dihydropteroate synthase in sulfadoxine-resistant malaria. EMBO J., 17, 3807-3815.
47. von Heijne, G. and Nishikawa, K. (1991) Chloroplast transit peptides: the perfect random coil? FEBS Lett., 278, 1-3.
48. Waegemann, K. and Soll, J. (1996) Phosphorylation of the transit sequence of chloroplast precursor proteins. J. Biol. Chem., 271, 6545-6554.
49. Waller, R.F., Keeling, P.J., Donald, R.G.K., Striepen, B., Handman, E., Lang-Unnasch, N., Cowman, A.F., Besra, G.S., Roos, D.S. and McFadden, G.I. (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 95, 12352-12357.
50. Wienk, H.L.J., Czisch, M. and de Kruijff, B. (1999) The structural flexibility of the preferredoxin transit peptide. FEBS Lett., 453, 318-326.
51. Wilson, R.J.M. et al. (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol., 261, 155-172.