Abstracts
Résumé
Le paludisme est responsable de plus de deux millions de décès par an, essentiellement en Afrique. Chez l’homme, le parasite infecte à la fois les hépatocytes et les érythrocytes, mais la symptomatologie de la maladie est seulement associée à l’infestation des globules rouges. Les érythrocytes matures sont à la fois incapables de synthèse de novo de protéines et dépourvus de tout type de transport intracellulaire. Aussi, pour sa survie, le parasite doit-il développer non seulement son propre transport vésiculaire, mais aussi un système membranaire qui lui permet de transporter les substances, dont les antigènes variants, jusqu’à la surface de l’érythrocyte. Quoique semblables au transport vésiculaire des mammifères dans leur régulation par les Rab GTPases, les systèmes membranaires développés par le parasite lui sont spécifiques et occupent même le cytosol de l’érythrocyte. La contribution des Rab codées par le parasite dans ce réseau sécrétoire élaboré est examinée dans cet article.
Summary
To survive within erythrocytes, Plasmodium parasites have to put into place different membrane and sub-cellular compartments in order to import different nutrients and to export proteins/antigens. Infected cells pose not only a major world health risk by killing two million people per year, but also a very interesting cell biology problem, as within the erythrocyte the parasite resides inside a vacuole called the parasitophorous vacuole and as a consequence, it is separated from the blood stream by three membrane barriers, its own plasma membrane, the parasitophorous vacuole membrane and the erythrocyte plasma membrane. In spite of these three barriers the parasite is capable of secreting antigens and importing nutrients, and to do this, it has developed a complex vesicular system that extends into the red blood cell cytoplasm to the plasma membrane. Understanding how the parasite controls this extensive vesicular traffic has driven research into Plasmodium Rabs, whose potential role is discussed.
Appendices
Références
- 1. Bannister LH, Hopkins JM, Fowler RE, et al. A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol Today 2000 ; 16 : 427-33.
- 2. Przyborski JM, Wickert H, Krohne G, et al. Maurer’s clefts : a novel secretory organelle ? Mol Biochem Parasitol 2003 ; 132 : 17-26.
- 3. Wickert H, Wissing F, Andrews KT, et al. Evidence for trafficking of PfEMP1 to the surface of P. falciparum-infected erythrocytes via a complex membrane network. Eur J Cell Biol 2003 ; 82 : 271-84.
- 4. Elmendorf HG, Haldar K. Plasmodium falciparum exports the Golgi marker sphingomyelin synthase into a tubovesicular network in the cytoplasm of mature erythrocytes. J Cell Biol 1994 ; 124 : 449-62.
- 5. Haeggstrom M, Kironde F, Berzins K, et al. Common trafficking pathway for variant antigens destined for the surface of the Plasmodium falciparum-infected erythrocyte. Mol Biochem Parasitol 2004 ; 133 : 1-14.
- 6. Albano FR, Foley M, Tilley L. Export of parasite proteins to the erythrocyte cytoplasm : secretory machinery and traffic signals. Novartis Found Symp 1999 ; 226 : 157-75.
- 7. Goodyer ID, Pouvelle B, Schneider TG, et al. Characterization of macromolecular transport pathways in malaria-infected erythrocytes. Mol Biochem Parasitol 1997 ; 87 : 13-28.
- 8. Waller RF, Reed MB, Cowman AF, et al. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 2000 ; 19 : 1794-802.
- 9. Cheresh P, Harrison T, Fujioka H, et al. Targeting the malarial plastid via the parasitophorous vacuole. J Biol Chem 2002 ; 277 : 16265-77.
- 10. Bender A, van Dooren GG, Ralph SA, et al. Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol Biochem Parasitol 2003 ; 132 : 59-66.
- 11. Klemba M, Beatty W, Gluzman I, et al. Trafficking of plasmepsin II to the food vacuole of the malaria parasite Plasmodium falciparum. J Cell Biol 2004 ; 164 : 47-56.
- 12. Ansorge I, Benting J, Bhakdi S, et al. Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem J 1996 ; 315 : 307-14.
- 13. Lingelbach K. Protein trafficking in the Plasmodium-falciparum-infected erythrocyte: from models to mechanisms. Ann Trop Med Parasitol 1997 ; 91 : 543-9.
- 14. Burghaus PA, Lingelbach K. Luciferase, when fused to an N-terminal signal peptide, is secreted from transfected Plasmodium falciparum and transported to the cytosol of infected erythrocytes. J Biol Chem 2001 ; 276 : 26838-45.
- 15. Adisa A, Rug M, Foley M, et al. Characterisation of a delta-COP homologue in the malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 2002 ; 123 : 11-21.
- 16. Wickham ME, Rug M, Ralph S, et al. Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J 2001 ; 20 : 5636-49.
- 17. Lopez-Estrano C, Bhattacharjee S, Harrison T, et al. Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci USA 2003 ; 100 : 12402-7.
- 18. Adisa A, Rug M, Klonis N, et al. 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 : 6532-42.
- 19. Taraschi TF, O’Donnell M, Martinez S, et al. Generation of an erythrocyte vesicle transport system by Plasmodium falciparum malaria parasites. Blood 2003 ; 102 : 3420-6.
- 20. Blisnick T, Morales Betoulle ME, Barale JC, et al. Pfsbp1, a Maurer’s cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol Biochem Parasitol 2000 ; 111 : 107-21.
- 21. Banumathy G, Singh V, Tatu U. Host chaperones are recruited in membrane-bound complexes by Plasmodium falciparum. J Biol Chem 2002 ; 277 : 3902-12.
- 22. Cooke BM, Lingelbach K, Bannister LH, et al. Protein trafficking in Plasmodium falciparum-infected red blood cells. Trends Parasitol 2004 ; 20 : 581-9.
- 23. Adisa A, Albano FR, Reeder J, et al. Evidence for a role for a Plasmodium falciparum homologue of Sec31p in the export of proteins to the surface of malaria parasite-infected erythrocytes. J Cell Sci 2001 ; 114 : 3377-86.
- 24. Hayashi M, Taniguchi S, Ishizuka Y, et al. 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. J Biol Chem 2001 ; 276 : 15249-55.
- 25. Spang A. Vesicle transport : a close collaboration of Rabs and effectors. Curr Biol 2004 ; 14 : R33-4.
- 26. Quevillon E, Spielmann T, Brahimi K, et al. The Plasmodium falciparum family of Rab GTPases. Gene 2003 ; 306 : 13-25.
- 27. Chakrabarti D, AzamT, DelVecchio C, et al. Protein prenyl transferase activities of Plasmodium falciparum. Mol Biochem Parasitol 1998 ; 94 : 175-84.
- 28. Attal G, Langsley G. A Plasmodium falciparum homologue of rab specific GDP dissociation inhibitor (rabGDI). Mol Biochem Parasitol 1996 ; 79 : 91-5.
- 29. Gotte M, Lazar T, Yoo JS, et al. The full complement of yeast Ypt/Rab-GTPases and their involvement in exo- and endocytic trafficking. Subcell Biochem 2000 ; 34 : 133-73.
- 30. Armstrong J, Craighead MW, Watson R, et al. Schizosaccharomyces pombe ypt5 : a homologue of the rab5 endosome fusion regulator. Mol Biol Cell 1993 ; 4 : 583-92.
- 31. Robibaro B, Stedman TT, Coppens I, et al. Toxoplasma gondii Rab5 enhances cholesterol acquisition from host cells. Cell Microbiol 2002 ; 4 : 139-52.
- 32. Singh SB, Tandon R, Krishnamurthy G, et al. Rab5-mediated endosome-endosome fusion regulates hemoglobin endocytosis in Leishmania donovani. EMBO J 2003 ; 22 : 5712-22.
- 33. Haldar K, Mohandas N, Samuel BU, et al. Protein and lipid trafficking induced in erythrocytes infected by malaria parasites. Cell Microbiol 2002 ; 4 : 383-95.
- 34. Moore RH, Millman EE, Alpizar-Foster E, et al. Rab11 regulates the recycling and lysosome targeting of beta2-adrenergic receptors. J Cell Sci 2004 ; 117 : 3107-17.
- 35. Harrison T, Samuel BU, Akompong T, et al. Erythrocyte G protein-coupled receptor signaling in malarial infection. Science 2003 ; 301 : 1734-6.
- 36. Marti M, Good RT, Rug M, et al. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 2004 ; 306 : 1930-3.
- 37. Hiller NL, Bhattacharjee S, van Ooij C, et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004 ; 306 : 1934-7.
- 38. Akompong T, Kadekoppala M, Harrison T, et al. Trans expression of a Plasmodium falciparum histidine-rich protein II (HRPII) reveals sorting of soluble proteins in the periphery of the host erythrocyte and disrupts transport to the malarial food vacuole. J Biol Chem 2002 ; 277 : 28923-33.
- 39. De Castro FA, Ward GE, Jambou R, et al. Identification of a family of Rab G-proteins in Plasmodium falciparum and a detailed characterisation of pfrab6. Mol Biochem Parasitol 1996 ; 80 : 77-88.
- 40. Gorlich D, Prehn S, Hartmann E, et al. A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell 1992 ; 71 : 489-503.
- 41. Dahl EL, Rosenthal PJ. Biosynthesis, localization, and processing of falcipain cysteine proteases of Plasmodium falciparum. Mol Biochem Parasitol 2005 ; 139 : 205-12.
- 42. Liu J, Gluzman IY, Drew ME, Goldberg DE. The role of Plasmodium falciparum food vacuole plasmepsins. J Biol Chem 2005 ; 280 : 1432-7.
- 43. Foth BJ, Stimmler LM, Handman E, et al. The malaria parasite Plasmodium falciparum has only one pyruvate dehydrogenase complex, which is located in the apicoplast. Mol Microbiol 2005 ; 55 : 39-53.
- 44. Yano K, Komaki-Yasuda K, Kobayashi T, et al. Expression of mRNAs and proteins for peroxiredoxins in Plasmodium falciparum erythrocytic stage. Parasitol Int 2005 ; 54 : 35-41.
- 45. Hodder AN, Drew DR, Epa VC, et al. Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5. J Biol Chem 2003 ; 278 : 48169-77.
- 46. Culvenor JG, Crewther PE. S-antigen localization in the erythrocytic stages of Plasmodium falciparum. J Protozool 1990 ;37 : 59-65.
- 47. Chen Q, Barragan A, Fernandez V, et al. Identification of Plasmodiumfalciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 1998 ; 187 : 15-23.
- 48. Kyes SA, Rowe JA, Kriek N, Newbold CI. Rifins : a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc Natl Acad Sci USA 1999 ; 96 : 9333-8.
- 49. Kaviratne M, Khan SM, Jarra W, Preiser PR. Small variant STEVOR antigen is uniquely located within Maurer’s clefts in Plasmodium falciparum-infected red blood cells. Eukaryot Cell 2002 ; 1 : 926-35.
- 50. Waller KL, Cooke BM, Nunomura W, et al. 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). J Biol Chem 1999 ; 274 : 23808-13.
- 51. Benedetti CE, Kobarg J, Pertinhez TA, et al. Plasmodium falciparum histidine-rich protein II binds to actin, phosphatidylinositol 4,5-bisphosphate and erythrocyte ghosts in a pH-dependent manner and undergoes coil-to-helix transitions in anionic micelles. Mol Biochem Parasitol 2003 ; 128 : 157-66.
- 52. Gardner MJ, Tettelin H, Carucci DJ, et al. Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Science 1998 ; 282 : 1126-32.
- 53. Spielmann T, Beck HP. Analysis of stage-specific transcription in Plasmodium falciparum reveals a set of genes exclusively transcribed in ring stage parasites. Mol Biochem Parasitol 2000 ; 111 : 453-8.
- 54. Langsley G, Chakrabarti D. Plasmodium falciparum : the small GTPase rab11. Exp Parasitol 1996 ; 83 : 250-1.
- 55. Hez-Deroubaix S, Brahimi K, Sauerwein R, et al. The Plasmodium falciparum GTPase Rab11B, a new liver-stage specific protein. Mol Biochem Parasitol 2005 (soumis pour publication).