Protein transport and trafficking in Plasmodium falciparum-infected erythrocytes

Parasitology

Volumn 130, Issue 4, 2005, Pages 373-388

  Przyborski, J M ^a   Lanzer, M ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Plasmodium falciparum; Protein trafficking; Signal sequences

Indexed keywords

APICOMPLEXA; APICOPLAST; CELL ORGANELLE; CYTOSOL; ENDOPLASMIC RETICULUM; ERYTHROCYTE; GOLGI COMPLEX; MALARIA; MITOCHONDRION; PARASITISM; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW;

ANIMALS; ANTIGENS, PROTOZOAN; ERYTHROCYTES; HUMANS; MALARIA, FALCIPARUM; ORGANELLES; PEPTIDES; PLASMODIUM FALCIPARUM; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SIGNAL TRANSDUCTION;

APICOMPLEXA; PLASMODIUM FALCIPARUM;

EID: 17144386621     PISSN: 00311820     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0031182004006729     Document Type: Review

References (174)

1. ADISA, A., ALBANO, F. R., REEDER, J., FOLEY, M. & TILLEY, L. (2001). Evidence for a role for a Plasmodium falciparum homologue of Sec31p in the export of proteins to the surface of malaria parasite-infected erythrocytes. Journal of Cell Science 114, 3377-3386.
2. ADISA, A., RUG, M., KLONIS, N., FOLEY, M., COWMAN, A. F. & TILLEY, L. (2003). The signal sequence of exported protein-1 directs the green fluorescent protein to the parasitophorous vacuole of transfected malaria parasites. Journal of Biological Chemistry 278, 6532-6542.
3. AIKAWA, M., MILLER, L. H., JOHNSON, J. & RABBEGE, J. (1978). Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. Journal of Cell Biology 77, 72-82.
4. ALBANO, F. R., BERMAN, A., LA GRECA, N., HIBBS, A. R., WICKHAM, M., FOLEY, M. & TILLEY, L. (1999). A homologue of Sar1p localises to a novel trafficking pathway in malaria-infected erythrocytes. European Journal of Cell Biology 78, 453-462.
5. ALBANO, F. R., FOLEY, M. & TILLEY, L. (1999). Export of parasite proteins to the erythrocyte cytoplasm: secretory-machinery and traffic signals. Novartis Foundation Symposium 226, 157-172; discussion 173-155.
6. ANIENTO, F., GU, F., PARTON, R. G. & GRUENBERG, J. (1996). An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. Journal of Cell Biology 133, 29-41.
7. ANSORGE, I., BENTING, J., BHAKDI, S. & LINGELBACH, K. (1996). Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochemical Journal 315, 307-314.
8. BALDI, D. L., ANDREWS, K. T., WALLER, R. F., ROOS, D. S., HOWARD, R. F., CRABB, B. S. & COWMAN, A. F. (2000). RAP controls rhoptry targeting of RAP2 in the malaria parasite Plasmodium falciparum. The EMBO Journal 19, 2435-2443.
9. BANUMATHY, G., SINGH, V. & TATU, U. (2002). Host chaperones are recruited in membrane-bound complexes by Plasmodium falciparum. Journal of Biological Chemistry 277, 3902-3912.
10. BARUCH, D. I., PASLOSKE, B. L., SINGH, H. B., BI, X., MA, X. C., FELDMAN, M., TARASCHI, T. F. & HOWARD, R. J. (1995). Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82, 77-87.
11. BEHARI, R. & HALDAR, K. (1994). Plasmodium falciparum: protein localization along a novel, lipid-rich tubovesicular membrane network in infected erythrocytes. Experimental Parasitology 79, 250-259.
12. BENDER, A., VAN DOOREN, G. G., RALPH, S. A., MCFADDEN, G. I. & SCHNEIDER, G. (2003). Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Molecular and Biochemical Parasitology 132, 59-66.
13. BENNETT, B. J., THOMPSON, J. & COPPEL, R. L. (1995). Identification of Plasmadium falciparum histone 2B and histone 3 genes. Molecular and Biochemical Parasitology 70, 231-233.
14. BIAGINI, G. A., BRAY, P. G., SPILLER, D. G., WHITE, M. R. & WARD, S. A. (2003). The digestive food vacuole of the malaria parasite is a dynamic intracellular Ca2+ store. Journal of Biological Chemistry 278, 27910-27915.
15. BIRAGO, C., ALBANESI, V., SILVESTRINI, F., PICCI, L., PIZZI, E., ALANO, P., PACE, T. & PONZI, M. (2003). A gene-family encoding small exported proteins is conserved across Plasmodium genus. Molecular and Biochemical Parasitology 126, 209-218.
16. BLACKMAN, M. J. & BANNISTER, L. H. (2001). Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Molecular and Biochemical Parasitology 117, 11-25.
17. BLISNICK, T., MORALES BETOULLE, M. E., BARALE, J. C., UZUREAU, P., BERRY, L., DESROSES, S., FUJIOKA, H., MATTEI, D. & BRAUN BRETON, C. (2000). Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Molecular and Biochemical Parasitology 111, 107-121.
18. BLOBEL, G. & DOBBERSTEIN, B. (1975a). Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. Journal of Cell Biology 67, 835-851.
19. BLOBEL, G. & DOBBERSTEIN, B. (1975b). Transfer to proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. Journal of Cell Biology 67, 852-862.
20. BLOBEL, G., WALTER, P., CHANG, C. N., GOLDMAN, B. M., ERICKSON, A. H. & LINGAPPA, V. R. (1979). Translocation of proteins across membranes: the signal hypothesis and beyond. Symposium of the Society for Experimental Biology 33, 9-36.
21. BOGERD, H. P., BENSON, R. E., TRUANT, R., HEROLD, A., PHINGBODHIPAKKIYA, M. & CULLEN, B. R. (1999). Definition of a consensus transportin-specific nucleocytoplasmic transport signal. Journal of Biological Chemistry 274, 9771-9777.
22. BORGHI, S., MOLINARI, S., RAZZINI, G., PARISH, F., BATTINI, R. & FERRARI, S. (2001). The nuclear localization domain of the MEF2 family of transcription factors shows member-specific features and mediates the nuclear import of histone deacetylase 4. Journal of Cell Science 114, 4477-4483.
23. BOZDECH, Z., DELLING, U., VOLKMAN, S. K., COWMAN, A. F. & SCHURR, E. (1996). Cloning and sequence analysis of a novel member of the ATP-binding cassette (ABC) protein gene family from Plasmodium falciparum. Molecular and Biochemical Parasitology 81, 41-51.
24. BRUCE, B. D. (2001). The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochimica et Biophysica Acta 1541, 2-21.
25. BURGHAUS, P.A. & LINGELBACH, K. (2001). Luciferase, when fused to an N-terminal signal peptide, is secreted from transfected Plasmodium falciparum and transported to the cytosol of infected erythrocytes. Journal of Biological Chemistry 276, 26838-26845.
26. CARRUTHERS, V. B. & SIBLEY, L. D. (1997). Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. European Journal of Cell Biology 73, 114-123.
27. CEREDE, O., DUBREMETZ, J. F., BOUT, D. & LEBRUN, M. (2002). The Toxoplasma gondii protein MIC3 requires propeptide cleavage and dimerization to function as adhesin. The EMBO Journal 21, 2526-2536.
28. CHENG, Q., CLOONAN, N., FISCHER, K., THOMPSON, J., WAINE, G., LANZER, M. & SAUL, A. (1998). Stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Molecular and Biochemical Parasitology 97, 161-176.
29. COPPEL, R. L. (1992). Repeat structures in a Plasmodium falciparum protein (MESA) that binds human erythrocyte protein 4.1. Molecular and Biochemical Parasitology 50, 335-347.
30. COUFFIN, S., HERNANDEZ-RIVAS, R., BLISNICK, T. & MATTEI, D. (1998). Characterisation of PfSec61, a Plasmodium falciparum homologue of a component of the translocation machinery at the endoplasmic reticulum membrane of eukaryotic cells. Molecular and Biochemical Parasitology 92, 89-98.
31. CRABB, B. S., COOKE, B. M., REEDER, J. C., WALLER, R. F., CARUANA, S. R., DAVERN, K. M., WICKHAM, M. E., BROWN, G. V., COPPEL, R. L. & COWMAN, A. F. (1997). Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89, 287-296.
32. CRABB, B. S., RUG, M., GILBERGER, T. W., THOMPSON, J. K., TRIGLIA, T., MAIER, A. G. & COWMAN, A. F. (2004). Transfection of the Human Malaria Parasite Plasmodium falciparum. Methods in Molecular Biology 270, 263-276.
33. CRAIG, A. & SCHERF, A. (2001). Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Molecular and Biochemical Parasitology 115, 129-143.
34. CREEDON, K. A., KASLOW, D. C., RATHOD, P. K. & WELLEMS, T. E. (1992). Identification of a Plasmodium falciparum histone 2A gene. Molecular and Biochemical Parasitology 54, 113-115.
35. CULVENOR, J. G., LANGFORD, C. J., CREWTHER, P. E., SAINT, R. B., COPPEL, R. L., KEMP, D. J., ANDERS, R. F. & BROWN, G. v. (1987). Plasmodium falciparum: identification and localization of a knob protein antigen expressed by a cDNA clone. Experimental Parasitology 63, 58-67.
36. DACKS, J. B. & DOOLITTLE, W. F. (2001). Reconstructing/deconstructing the earliest eukaryotes: how comparative genomics can help. Cell 107, 419-425.
37. DANG, C. V. & LEE, W. M. (1988). Identification of the human c-myc protein nuclear translocation signal. Molecular and Cellular Biology 8, 4048-4054.
38. DE CASTRO, F. A., WARD, G. E., JAMBOU, R., ATTAL, G., MAYAU, V., JAUREGUIBERRY, G., BRAUN-BRETON, C., CHAKRABARTI, D. & LANGSLEY, G. (1996). Identification of a family of Rab G-proteins in Plasmodium falciparum and a detailed characterisation of pfrabo. Molecular and Biochemical Parasitology 80, 77-88.
39. DEITSCH, K., DRISKILL, C. & WELLEMS, T. (2001). Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Research 29, 850-853.
40. DI CRISTINA, M., SPACCAPELO, R., SOLDATI, D., BISTONI, F. & CRISANTI, A. (2000). Two conserved amino acid motifs mediate protein targeting to the micronemes of the apicomplexan parasite Toxoplasma gondii. Molecular and Cellular Biology 20, 7332-7341.
41. DUBREMETZ, J. F. & SCHWARTZMAN, J. D. (1993). Subcellular organelles of Toxoplasma gondii and host cell invasion. Research in Immunology 144, 31-33.
42. ELFORD, B. C., COWAN, G. M. & FERGUSON, D. J. (1995). Parasite-regulated membrane transport processes and metabolic control in malaria-infected erythrocytes. The Biochemical Journal 308, 361-374.
43. ELMENDORF, H. G. & HALDAR, K. (1993). Identification and localization of ERD2 in the malaria parasite Plasmodium falciparum: separation from sites of sphingomyelin synthesis and implications for organization of the Golgi. The EMBO Journal 12, 4763-4773.
44. ETZION, Z. & PERKINS, M. E. (1989). Localization of a parasite encoded protein to erythrocyte cytoplasmic vesicles of Plasmodium falciparum-infected cells. European Journal of Cell Biology 48, 174-179.
45. FAN, Q., AN, L. & CUI, L. (2004). Plasmodium falciparum histone acetyltransferase, a yeast GCN5 homologue involved in chromatin remodeling. Eukaryotic Cell 3, 264-276.
46. FAVALORO, J. M., COPPEL, R. L., CORCORAN, L. M., FOOTE, S. J., BROWN, G. V., ANDERS, R. F. & KEMP, D. J. (1986). Structure of the RESA gene of Plasmodium falciparum. Nucleic Acids Research 14, 8265-8277.
47. FIELD, M. C., ALI, B. R. & FIELD, H. (1999). GTPases in protozoan parasites : tools for cell biology and chemotherapy. Parasitology Today 15, 365-371.
48. FOLEY, M. & TILLEY, L. (1998a). Protein trafficking in malaria-infected erythrocytes. International Journal for Parasitology 28, 1671-1680.
49. FOLEY, M. & TILLEY, L. (1998b). Quinoline antimalarials: mechanisms of action and resistance and prospects for new agents. Pharmacology and Therapeutics 79, 55-87.
50. FOTH, B. J. & MCFADDEN, G. I. (2003). The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. International Review of Cytology 224, 57-110.
51. FOTH, B. J., RALPH, S. A., TONKIN, C. J., STRUCK, N. S., FRAUNHOLZ, M., ROOS, D.S., COWMAN, A. F. & MCFADDEN, G. I. (2003). Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299, 705-708.
52. GILBERGER, T. W., THOMPSON, J. K., REED, M. B., GOOD, R. T. & COWMAN, A. F. (2003). The cytoplasmic domain of the Plasmodium falciparum ligand EBA-175 is essential for invasion but not protein trafficking. Journal of Cell Biology 162, 317-327.
53. GILSON, P. R. & MCFADDEN, G. I. (2002). Jam packed genomes - a preliminary, comparative analysis of nucleomorphs. Genetica 115, 13-28.
54. GINSBURG, H., FAMIN, O., ZHANG, J. & KRUGLIAK, M. (1998). Inhibition of glutathione-dependent degradation of heme by chloroquine and amodiaquine as a possible basis for their antimalarial mode of action. Biochemical Pharmacology 56, 1305-1313.
55. GORLICH, D. & MATTAJ, I. W. (1996). Nucleocytoplasmic transport. Science 271, 1513-1518.
56. GU, F., ANIENTO, F., PARTON, R. G. & GRUENBERG, J. (1997). Functional dissection of COP-I subunits in the biogenesis of multivesicular endosomes. Journal of Cell Biology 139, 1183-1195.
57. GUNTHER, K., TUMMLER, M., ARNOLD, H.H., RIDLEY, R., GOMAN, M., SCAIFE, J. G. & LINGELBACH, K. (1991). An exported protein of Plasmodium falciparum is synthesized as an integral membrane protein. Molecular and Biochemical Parasitology 46, 149-157.
58. HAGER, K., STRIEPEN, B., TILNEY, L. & ROOS, D. (1999). The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. Journal of Cell Science 112, 2631-2638.
59. HALDAR, K., SAMUEL, B. U., MOHANDAS, N., HARRISON, T. & HILLER, N. L. (2001). Transport mechanisms in Plasmodium-infected erythrocytes: lipid rafts and a tubovesicular network. International Journal for Parasitology 31, 1393-1401.
60. HAWTHORNE, P. L., TRENHOLME, K. R., SKINNER-ADAMS, T. S., SPIELMANN, T., FISCHER, K., DIXON, M. W. A., ORTEGA, M. R., ANDERSON, K. L., KEMP, D. J. & GARDINER, D. L. (2004). A novel Plasmodium falciparum ring stage protein, REX, is located in Maurer's clefts. Molecular and Biochemical Parasitology 136, 181-189.
61. HAYASHI, M., TANIGUCHI, S., ISHIZUKA, Y., KIM, H. S., WATAYA, Y., YAMAMOTO, A. & MORIYAMA, Y. (2001). A homologue of N-ethylmaleimide- sensitive factor in the malaria parasite Plasmodium falciparum is exported and localized in vesicular structures in the cytoplasm of infected erythrocytes in the brefeldin A-sensitive pathway. Journal of Biological Chemistry 276, 15249-15255.
62. HEHL, B. & MARTI, M. (2004). Secretory protein trafficking in Giardia intestinalis. Molecular Microbiology 53, 19-28.
63. HIBBS, A. R. & SAUL, A. J. (1994). Plasmodium falciparum: highly mobile small vesicles in the malaria-infected red blood cell cytoplasm. Experimental Parasitology 79, 260-269.
64. HOLT, D. C., GARDINER, D. L., THOMAS, E. A., MAYO, M., BOURKE, P. F., SUTHERLAND, C. J., CARTER, R., MYERS, G., KEMP, D. J. & TRENHOLME, K. R. (1999). The cytoadherence linked asexual gene family of Plasmodium falciparum: are there roles other than cytoadherence? International Journal for Parasitology 29, 939-944.
65. HOOGENRAAD, N. J., WARD, L. A. & RYAN, M. T. (2002). Import and assembly of proteins into mitochondria of mammalian cells. Biochimica et Biophysica Acta 1592, 97-105.
66. HOPPE, H. C. & JOINER, K. A. (2000). Cytoplasmic tail motifs mediate endoplasmic reticulum localization and export of transmembrane reporters in the protozoan parasite Toxoplasma gondii. Cellular Microbiology 2, 569-578.
67. HOPPE, H. C., NGO, H. M., YANG, M. & JOINER, K. A. (2000). Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionarily conserved mechanisms. Nature Cell Biology 2, 449-456.
68. HOWARD, R., LYON, J., UNI, S., SAUL, A., ALEY, S., KLOTZ, F., PANTON, L., SHERWOOD, J., MARSH, K. & AIKAWA, M. (1987). Transport of an Mr approximately 300,000 Plasmodium falciparum protein (Pf EMP 2) from the intraerythrocytic asexual parasite to the cytoplasmic face of the host cell membrane. Journal of Cell Biology 104, 1269-1280.
69. HOWARD, R. F. & REESE, R. T. (1990). Plasmodium falciparum: hetero-oligomeric complexes of rhoptry polypeptides. Experimental Parasitology 71, 330-342.
70. JACKSON, M. R., NILSSON, T. & PETERSON, P. A. (1990). Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. The EMBO Journal 9, 3153-3162.
71. JACKSON, M. R., NILSSON, T. & PETERSON, P. A. (1993). Retrieval of transmembrane proteins to the endoplasmic reticulum. Journal of Cell Biology 121, 317-333.
72. JOSHI, M. B., LIN, D. T., CHIANG, P. H., GOLDMAN, N. D., FUJIOKA, H., AIKAWA, M. & SYIN, C. (1999). Molecular cloning and nuclear localization of a histone deacetylase homologue in Plasmodium falciparum. Molecular and Biochemical Parasitology 99, 11-19.
73. KALIES, K. U. & HARTMANN, E. (1998). Protein translocation into the endoplasmic reticulum (ER) - two similar routes with different modes. European Journal of Biochemistry 254, 1-5.
74. KAVIRATNE, M., KHAN, S. M., JARRA, W. & PREISER, P. R. (2002). Small variant STEVOR antigen is uniquely located within Maurer's clefts in Plasmodium falciparum-infected red blood cells. Eukaryotic Cell 1, 926-935.
75. KILEJIAN, A. (1979). Characterization of a protein correlated with the production of knob-like protrusions on membranes of erythrocytes infected with Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 76, 4650-4653.
76. KIRCHHAUSEN, T. (2000). Three ways to make a vesicle. Nature Reviews Molecular Cell Biology 1, 187-198.
77. KIRK, K. (2004). Channels and transporters as drug targets in the Plasmodium-infected erythrocyte. Acta Tropica 89, 285-298.
78. KIRK, K., TILLEY, L. & GINSBURG, H. (1999). Transport and trafficking in the malaria-infected erythrocyte. Parasitology Today 15, 355-357.
79. KLEMBA, M., BEATTY, W., GLUZMAN, I. & GOLDBERG, D. E. (2004). Trafficking of plasmepsin II to the food vacuole of the malaria parasite Plasmodium falciparum. Journal of Cell Biology 164, 47-56.
80. KNAPP, B., HUNDT, E. & KUPPER, H. A. (1989). A new blood stage antigen of Plasmodium falciparum transported to the erythrocyte surface. Molecular and Biochemical Parasitology 37, 47-56.
81. KOCKEN, C. H., VAN DER WEL, A. M., DUBBELD, M. A., NARUM, D. L., VAN DE RIJKE, F. M., VAN GEMERT, G. J., VAN DER LINDE, X., BANNISTER, L. H., JANSE, C., WATERS, A. P. & THOMAS, A. W. (1998). Precise timing of expression of a Plasmodium falciparum-derived transgene in Plasmodium berghei is a critical determinant of subsequent subcellular localization. Journal of Biological Chemistry 273, 15119-15124.
82. KOHLER, S., DELWICHE, C. F., DENNY, P. W., TILNEY, L. G., WEBSTER, P., WILSON, R. J., PALMER, J. D. & ROOS, D. S. (1997). A plastid of probable green algal origin in Apicomplexan parasites. Science 275, 1485-1489.
83. KRIEK, N., TILLEY, L., HORROCKS, P., PINCHES, R., ELFORD, B. C., FERGUSON, D. J., LINGELBACH, K. & NEWBOLD, C. I. (2003). Characterization of the pathway for transport of the cytoadherence-mediating protein, PfEMP1, to the host cell surface in malaria parasite-infected erythrocytes. Molecular Microbiology 50, 1215-1227.
84. KUMAR, N., KOSKI, G., HARADA, M., AIKAWA, M. & ZHENG, H. (1991). Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Molecular and Biochemical Parasitology 48, 47-58.
85. LAGRECA, N., HIBBS, A. R., RIFFKIN, C., FOLEY, M. & TILLEY, L. (1997). Identification of an endoplasmic reticulum-resident calcium-binding protein with multiple EF-hand motifs in asexual stages of Plasmodium falciparum. Molecular and Biochemical Parasitology 89, 283-293.
86. LANFORD, R. E., KANDA, P. & KENNEDY, R. C. (1986). Induction of nuclear transport with a synthetic peptide homologous to the SV40 T antigen transport signal. Cell 46, 575-582.
87. LAUER, S. A., RATHOD, P. K., GHORI, N. & HALDAR, K. (1997). A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276, 1122-1125.
88. LETOURNEUR, F., GAYNOR, E. C., HENNECKE, S., DEMOLLIERE, C., DUDEN, R., EMR, S. D., RIEZMAN, H. & COSSON, P. (1994). Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199-1207.
89. LEW, V. L., TIFFERT, T. & GINSBURG, H. (2003). Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells. Blood 101, 4189-4194.
90. LEWIS, M. J. & PELHAM, H. R. (1990). A human homologue of the yeast HDEL receptor. Nature, London 348, 162-163.
91. LEWIS, M. J. & PELHAM, H. R. (1992). Sequence of a second human KDEL receptor. Journal of Molecular Biology 226, 913-916.
92. LEWIS, M. J., SWEET, D. J. & PELHAM, H. R. (1990). The ERD2 gene determines the specificity of the luminal ER protein retention system. Cell 61, 1359-1363.
93. LILL, R. & NEUPERT, W. (1996). Mechanisms of protein import across the mitochondrial outer membrane. Trends in Cell Biology 6, 56-61.
94. LING, I. T., FLORENS, L., DLUZEWSKI, A. R., KANEKO, O., GRAINGER, M., YIM LIM, B. Y., TSUBOI, T., HOPKINS, J. M., JOHNSON, J. R., TORII, M., BANNISTER, L. H., YATES, J. R., 3RD, HOLDER, A. A. & MATTEI, D. (2004). The Plasmodium falciparum clag9 gene encodes a rhoptry protein that is transferred to the host erythrocyte upon invasion. Molecular Microbiology 52, 107-118.
95. LINGELBACH, K. (1997). Protein trafficking in the Plasmodium-falciparum- infected erythrocyte - from models to mechanisms. Annals of Tropical Medicine and Parasitology 91, 543-549.
96. LINGELBACH, K. R. (1993). Plasmodium falciparum: a molecular view of protein transport from the parasite into the host erythrocyte. Experimental Parasitology 76, 318-327.
97. LOPEZ-ESTRANO, C., BHATTACHARJEE, S., HARRISON, T. & HALDAR, K. (2003). Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum-infected erythrocytes. Proceedings of the National Academy of Sciences, USA 100, 12402-12407.
98. LORIA, P., MILLER, S., FOLEY, M. & TILLEY, L. (1999). Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. The Biochemical Journal 339 (Pt 2), 363-370.
99. LUSTIGMAN, S., ANDERS, R. F., BROWN, G. V. & COPPEL, R. L. (1988). A component of an antigenic rhoptry complex of Plasmodium falciparum is modified after merozoite invasion. Molecular and Biochemical Parasitology 30, 217-224.
100. MACASEV, D., WHELAN, J., NEWBIGIN, E., SILVA-FILHO, M. C., MULHERN, T. D. & LITHGOW, T. (2004). Tom22', an 8 kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes. Molecular Biology and Evolution 21, 1557-1564.
101. MAGOWAN, C., NUNOMURA, W., WALLER, K. L., YEUNG, J., LIANG, J., VAN DORT, H., LOW, P. S., COPPEL, R. L. & MOHANDAS, N. (2000). Plasmodium falciparum histidine-rich protein 1 associates with the band 3 binding domain of ankyrin in the infected red cell membrane. Biochimica et Biophysica Acta 1502, 461-470.
102. MANNING-CELA, R., MARQUEZ, C., FRANCO, E., TALAMAS-ROHANA, P. & MEZA, I. (2003). BFA-sensitive and insensitive exocytic pathways in Entamoeba histolytica trophozoites: their relationship to pathogenesis. Cellular Microbiology 5, 921-932.
103. MATTEI, D., BERRY, L., COUFFIN, S. & RICHARD, O. (1999). The transport of the histidine-rich protein I from Plasmodium falciparum is insensitive to brefeldin A. Novartis Foundation Symposium 226, 215-226; discussion 227-230.
104. MATTEI, D. & SCHERF, A. (1992a). The Pf332 gene codes for a megadalton protein of Plasmodium falciparum asexual blood stages. Memorias do Institito Oswaldo Cruz 87 (Suppl. 3), 163-168.
105. MATTEI, D. & SCHERF, A. (1992b). The Pf332 gene of Plasmodium falciparum codes for a giant protein that is translocated from the parasite to the membrane of infected erythrocytes. Gene 110, 71-79.
106. MAYER, A. & WICKNER, W. (1997). Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). Journal of Cell Biology 136, 307-317.
107. MILLER, L. H., BARUCH, D. I., MARSH, K. & DOUMBO, O. K. (2002). The pathogenic basis of malaria. Nature, London 415, 673-679.
108. MIURA, S., KASUYA-ARAI, I., MORI, H., MIYAZAWA, S., OSUMI, T., HASHIMOTO, T. & FUJIKI, Y. (1992). Carboxyl-terminal consensus Ser-Lys-Leu-related tripeptide of peroxisomal proteins functions in vitro as a minimal peroxisome-targeting signal. Journal of Biological Chemistry 267, 14405-14411.
109. MOHMMED, A., KISHORE, S., DASARADHI, P. V., PATRA, K., MALHOTRA, P. & CHAUHAN, V. S. (2003). Cloning and characterization of Plasmodium falciparum homologs of nuclear import factors, karyopherin alpha and karyopherin beta. Molecular and Biochemical Parasitology 127, 199-203.
110. NACER, A., BERRY, L., SLOMIANNY, C. & MATTEI, D. (2001). Plasmodium falciparum signal sequences: simply sequences or special signals? International Journal for Parasitology 31, 1371-1379.
111. NAKAI, K. & HORTON, P. (1999). PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends in Biochemical Sciences 24, 34-36.
112. NEUPERT, W. & BRUNNER, M. (2002). The protein import motor of mitochondria. Nature Reviews Molecular Cell Biology 3, 555-565.
113. NGO, H. M., YANG, M., PAPROTKA, K., PYPAERT, M., HOPPE, H. & JOINER, K. A. (2003). AP-1 in Toxoplasma gondii mediates biogenesis of the rhoptry secretory organelle from a post-Golgi compartment. Journal of Biological Chemistry 278, 5343-5352.
114. NIKAIDO, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews 67, 593-656.
115. NILSSON, T., JACKSON, M. & PETERSON, P. A. (1989). Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58, 707-718.
116. NILSSON, T. & WARREN, G. (1994). Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Current Opinions in Cell Biology 6, 517-521.
117. NOLTE, D., HUNDT, E., LANGSLEY, G. & KNAPP, B. (1991). A Plasmodium falciparum blood stage antigen highly homologous to the glycophorin binding protein GBP. Molecular and Biochemical Parasitology 49, 253-264.
118. O'DONNELL, R. A., FREITAS-JUNIOR, L. H., PREISER, P. R., WILLIAMSON, D.H., DURAISINGH, M., MCELWAIN, T. F., SCHERF, A., COWMAN, A. F. & CRABB, B. S. (2002). A genetic screen for improved plasmid segregation reveals a role for Rep20 in the interaction of Plasmodium falciparum chromosomes. The EMBO Journal 21, 1231-1239.
119. ORCI, L., STAMNES, M., RAVAZZOLA, M., AMHERDT, M., PERRELET, A., SOLLNER, T. H. & ROTHMAN, J. E. (1997). Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335-349.
120. OSTERMANN, J., ORCI, L., TANI, K., AMHERDT, M., RAVAZZOLA, M., ELAZAR, Z. & ROTHMAN, J. E. (1993). Stepwise assembly of functionally active transport vesicles. Cell 75, 1015-1025.
121. PAGOLA, S., STEPHENS, P. W., BOHLE, D. S., KOSAR, A. D. & MADSEN, S. K. (2000). The structure of malaria pigment beta-haematin. Nature 404, 307-310.
122. PANTON, L. J., MCPHIE, P., MALOY, W. L., WELLEMS, T. E., TAYLOR, D.W. & HOWARD, R. J. (1989). Purification and partial characterization of an unusual protein of Plasmodium falciparum: histidine-rich protein II. Molecular and Biochemical Parasitology 35, 149-160.
123. PAPALEXIS, V., SIOMOS, M. A., CAMPANALE, N., GUO, X., KOCAK, G., FOLEY, M. & TILLEY, L. (2001). Histidine-rich protein 2 of the malaria parasite, Plasmodium falciparum, is involved in detoxification of the by-products of haemoglobin degradation. Molecular and Biochemical Parasitology 115, 77-86.
124. PEPPERKOK, R., SCHEEL, J., HORSTMANN, H., HAURI, H. P., GRIFFITHS, G. & KREIS, T. E. (1993). Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell 74, 71-82.
125. PETERSON, M. G., CREWTHER, P. E., THOMPSON, J. K., CORCORAN, L. M., COPPEL, R. L., BROWN, G. V., ANDERS, R. F. & KEMP, D. J. (1988). A second antigenic heat shock protein of Plasmodium falciparum. DNA 7, 71-78.
126. PETERSON, M. G., MARSHALL, V. M., SMYTHE, J. A., CREWTHER, P. E., LEW, A., SILVA, A., ANDERS, R. F. & KEMP, D. J. (1989). Integral membrane protein located in the apical complex of Plasmodium falciparum. Molecular and Cellular Biology 9, 3151-3154.
127. POLOGE, L. G., PAVLOVEC, A., SHIO, H. & RAVETCH, J. V. (1987). Primary structure and subcellular localization of the knob-associated histidine-rich protein of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 84, 7139-7143.
128. PRZYBORSKI, J. M., BARTELS, K., LANZER, M. & ANDREWS, K. T. (2003a). The histone H4 gene of Plasmodium falciparum is developmentally transcribed in asexual parasites. Parasitology Research 90, 387-389.
129. PRZYBORSKI, J. M., WICKERT, H., KROHNE, G. & LANZER, M. (2003b). Maurer's clefts - a novel secretory organelle? Molecular and Biochemical Parasitology 132, 17-26.
130. REISS, M., VIEBIG, N., BRECHT, S., FOURMAUX, M. N., SOETE, M., DI CRISTINA, M., DUBREMETZ, J. F. & SOLDATI, D. (2001). Identification and characterization of an escorter for two secretory adhesins in Toxoplasma gondii. Journal of Cell Biology 152, 563-578.
131. ROBBINS, J., DILWORTH, S. M., LASKEY, R. A. & DINGWALL, C. (1991). Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64, 615-623.
132. ROBINSON, M. S. (1994). The role of clathrin, adaptors and dynamin in endocytosis. Current Opinions in Cell Biology 6, 538-544.
133. RODRIGUE, A., CHANAL, A., BECK, K., MULLER, M. & WU, L. F. (1999). Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. Journal of Biological Chemistry 274, 13223-13228.
134. ROOS, D. S., CRAWFORD, M. J., DONALD, R. G., FOHL, L. M., HAGER, K. M., KISSINGER, J. C., REYNOLDS, M. G., STRIEPEN, B. & SULLIVAN, W. J., Jr. (1999). Transport and trafficking: Toxoplasma as a model for Plasmodium. Novartis Foundation Symposium 226, 176-195; discussion 195-178.
135. ROOS, D. S., CRAWFORD, M. J., DONALD, R. G., FRAUNHOLZ, M., HARB, O. S., HE, C. Y., KISSINGER, J. C., SHAW, M. K. & STRIEPEN, B. (2002). Mining the Plasmodium genome database to define organellar function: what does the apicoplast do? Philosophical Transactions of the Royal Society of London, Series B 357, 35-46.
136. SAM-YELLOWE, T. Y., FLORENS, L., JOHNSON, J. R., WANG, T., DRAZBA, J. A., LE ROCH, K. G., ZHOU, Y., BATALOV, S., CARUCCI, D. J., WINZELER, E. A. & YATES, J, R., 3RD. (2004). A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Research 14, 1052-1059.
137. SATO, S., CLOUGH, B., COATES, L. & WILSON, R. J. (2004). Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist 155, 117-125.
138. SATO, S., RANGACHARI, K. & WILSON, R. J. (2003). Targeting GFP to the malarial mitochondrion. Molecular and Biochemical Parasitology 130, 155-158.
139. SATO, S. & WILSON, R. J. (2004). The use of DsRED in single- and dual-color fluorescence labeling of mitochondrial and plastid organelles in Plasmodium falciparum. Molecular and Biochemical Parasitologv 134, 175-179.
140. SAUL, A., COOPER, J., HAUQUITZ, D., IRVING, D., CHENG, Q., STOWERS, A. & LIMPAIBOON, T. (1992). The 42-kilodalton rhoptry-associated protein of Plasmodium falciparum. Molecular and Biochemical Parasitology 50, 139-149.
141. SAUL, A., YEGANEH, F. & HOWARD, R. J. (1992). Conservation of repeating structures in the PFEMP2/MESA protein of Plasmodium falciparum. Immunology and Cell Biology 70, 353-355.
142. SERAFINI, T., STENBECK, G., BRECHT, A., LOTTSPEICH, F., ORCI, L., ROTHMAN, J. E. & WIELAND, F. T. (1991). A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin. Nature, London 349, 215-220.
143. SIMMONS, D., WOOLLETT, G., BERGIN-CARTWRIGHT, M., KAY, D. & SCAIFE, J. (1987). A malaria protein exported into a new compartment within the host erythrocyte. The EMBO Journal 6, 485-491.
144. SMITH, J. D., CHITNIS, C. E., CRAIG, A. G., ROBERTS, D. J., HUDSON-TAYLOR, D. E., PETERSON, D. S., PINCHES, R., NEWBOLD, C. I. & MILLER, L. H. (1995). Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82, 101-110.
145. SOLL, J. & SCHLEIFF, E. (2004). Protein import into chloroplasts. Nature Reviews Molecular Cell Biology 5, 198-208.
146. SPIELMANN, T., FERGUSEN, D. J. & BECK, H. P. (2003). Etramps, a new Plasmodium falciparum gene family coding for developmentally regulated and highly charged membrane proteins located at the parasite-host cell interface. Molecular Biology of the Cell 14, 1529-1544.
147. SPYCHER, C., KLONIS, N., SPIELMANN, T., KUMP, E., STEIGER, S., TILLEY, L. & BECK, H. P. (2003). MAHRP-1, a novel Plasmodium falciparum histidine-rich protein, binds ferriprotoporphyrin IX and localises to the Maurer's clefts. Journal of Biological Chemistry 278, 35373-35383.
148. STENZEL, D. J. & KARA, U. A. (1989). Sorting of malarial antigens into vesicular compartments within the host cell cytoplasm as demonstrated by immunoelectron microscopy. European Journal of Cell Biology 49, 311-318.
149. SU, X. Z., HEATWOLE, V. M., WERTHEIMER, S. P., GUINET, F., HERRFELDT, J. A., PETERSON, D. S., RAVETCH, J. A. & WELLEMS, T. E. (1995). The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82, 89-100.
150. SYIN, C. & GOLDMAN, N. D. (1996). Cloning of a Plasmodium falciparum gene related to the human 60-kDa heat shock protein. Molecular and Biochemical Parasitology 79, 13-19.
151. TARASCHI, T. F., O'DONNELL, M., MARTINEZ, S., SCHNEIDER, T., TRELKA, D., FOWLER, V. M., TILLEY, L. & MORIYAMA, Y. (2003). Generation of an erythrocyte vesicle transport system by Plasmodium falciparum malaria parasites. Blood 102, 3420-3426.
152. TARASCHI, T. F., TRELKA, D., MARTINEZ, S., SCHNEIDER, T. & O'DONNELL, M. E. (2001). Vesicle-mediated trafficking of parasite proteins to the host cell cytosol and erythrocyte surface membrane in Plasmodium falciparum infected erythrocytes. International Journal for Parasitology 31, 1381-1391.
153. TAYLOR, D. W., PARRA, M., CHAPMAN, G. B., STEARNS, M. E., RENER, J., AIKAWA, M., UNI, S., ALEY, S. B., PANTON, L. J. & HOWARD, R. J. (1987). Localization of Plasmodium falciparum histidine-rich protein 1 in the erythrocyte skeleton under knobs. Molecular and Biochemical Parasitology 25, 165-174.
154. TRELKA, D. P., SCHNEIDER, T. G., REEDER, J. C. & TARASCHI, T. F. (2000). Evidence for vesicle-mediated trafficking of parasite proteins to the host cell cytosol and erythrocyte surface membrane in Plasmodium falciparum infected erythrocytes. Molecular and Biochemical Parasitology 106, 131-145.
155. TRUSCOTT, K. N., BRANDNER, K. & PFANNER, N. (2003). Mechanisms of protein import into mitochondria. Current Biology 13, R326-337.
156. VAN DOOREN, G. G., SU, V., D'OMBRAIN, M. C. & MCFADDEN, G. I. (2002). Processing of an apicoplast leader sequence in Plasmodium falciparum and the identification of a putative leader cleavage enzyme. Journal of Biological Chemistry 277, 23612-23619.
157. VAN WYE, J., GHORI, N., WEBSTER, P., MITSCHLER, R. R., ELMENDORF, H. G. & HALDAR, K. (1996). Identification and localization of rab6, separation of rab6 from ERD2 and implications for an 'unstacked' Golgi, in Plasmodium falciparum. Molecular and Biochemical Parasitology 83, 107-120.
158. WALLER, K. L., COOKE, B. M., NUNOMURA, W., MOHANDAS, N. & COPPEL, R. L. (1999). 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). Journal of Biological Chemistry 274, 23808-23813.
159. WALLER, K. L., NUNOMURA, W., COOKE, B. M., MOHANDAS, N. & COPPEL, R. L. (2002). Mapping the domains of the cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) that bind to the knob-associated histidine-rich protein (KAHRP). Molecular and Biochemical Parasitology 119, 125-129.
160. WALLER, R. F., KEELING, P. J., DONALD, R. G., STRIEPEN, B., HANDMAN, E., LANG-UNNASCH, N., COWMAN, A. F., BESRA, G. S., ROOS, D. S. & MCFADDEN, G. I. (1998). Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 95, 12352-12357.
161. WALLER, R. F., KEELING, P. J., VAN DOOREN, G. G. & MCFADDEN, G. I. (2003). Comment on "A green algal apicoplast ancestor". Science 301, 49.
162. WALLER, R. F., REED, M. B., COWMAN, A. F. & MCFADDEN, G. I. (2000). Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. The EMBO Journal 19, 1794-1802.
163. WARHURST, D. C., CRAIG, J. C. & ADAGU, I. S. (2002). Lysosomes and drug resistance in malaria. Lancet 360, 1527-1529.
164. WATERKEYN, J. G., WICKHAM, M. E., DAVERN, K. M., COOKE, B. M., COPPEL, R. L., REEDER, J. C., CULVENOR, J. G., WALLER, R. F. & COWMAN, A. F. (2000). Targeted mutagenesis of Plasmodium falciparum erythrocyte membrane protein 3 (PfEMP3) disrupts cytoadherence of malaria-infected red blood cells. The EMBO Journal 19, 2813-2823.
165. WATERS, M. G., SERAFINI, T. & ROTHMAN, J. E. (1991). 'Coatomer': a cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature, London 349, 248-251.
166. WEIGHARDT, F., BIAMONTI, G. & RIVA, S. (1995). Nucleocytoplasmic distribution of human hnRNP proteins: a search for the targeting domains in hnRNP A1. Journal of Cell Science 108, 545-555.
167. WHITNEY, J. A., GOMEZ, M., SHEFF, D., KREIS, T. E. & MELLMAN, I. (1995). Cytoplasmic coat proteins involved in endosome function. Cell 83, 703-713.
168. WICKERT, H., ROHRBACH, P., SCHERER, S., KROHNE, G. & LANZER, M. (2003a). A putative Sec23 homologue of Plasmodium falciparum is located in Maurer's clefts. Molecular and Biochemical Parasitology 129, 209-213.
169. WICKERT, H., WISSING, F., ANDREWS, K. T., STICH, A., KROHNE, G. & LANZER, M. (2003b). Evidence for trafficking of PfEMP1 to the surface of P. falciparum-infected erythrocytes via a complex membrane network. European Journal of Cell Biology 82, 271-284.
170. WICKHAM, M. E., RUG, M., RALPH, S. A., KLONIS, N., MCFADDEN, G. I., TILLEY, L. & COWMAN, A. F. (2001). Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. The EMBO Journal 20, 5636-5649.
171. WINSTANLEY, P. (2001). Modern chemotherapeutic options for malaria. Lancet Infectious Diseases 1, 242-250.
172. WISER, M. F., LANNERS, H. N., BAFFORD, R. A. & FAVALORO, J. M. (1997). A novel alternate secretory pathway for the export of Plasmodium proteins into the host erythrocyte. Proceedings of the National Academy of Sciences, USA 94, 9108-9113.
173. WRENGER, C. & MÜLLER, S. (2004). The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoylation pathways. Molecular Microbiology 53, 103-113.
174. XU, X., YAMASAKI, H., FENG, Z. & AOKI, T. (2002). Molecular cloning and characterization of Plasmodium falciparum transportin. Parasitology Research 88, 391-394.