Proteomic analysis of detergent-Resistant membrane microdomains in trophozoite blood stage of the human malaria parasite plasmodium falciparum

Molecular and Cellular Proteomics

Volumn 12, Issue 12, 2013, Pages 3948-3961

  Yam, Xue Yan ^a,d   Birago, Cecilia ^b   Fratini, Federica ^b   Di Girolamo, Francesco ^b   Raggi, Carla ^b   Sargiacomo, Massimo ^b   Bachi, Angela ^c   Berry, Laurence ^a   Fall, Gamou ^a   Currà, Chiara ^b   Pizzi, Elisabetta ^b   Breton, Catherine Braun ^a   Ponzi, Marta ^b  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; DETERGENT; LIPID; PHOSPHOLIPID; PROTOZOAL PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; CYTOSOL; DENSITY GRADIENT CENTRIFUGATION; ENDOPLASMIC RETICULUM; ERYTHROCYTE; GENE EXPRESSION PROFILING; LIPID ANALYSIS; MEMBRANE STRUCTURE; MITOCHONDRION; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTEOMICS; SURFACE PROPERTY; TROPHOZOITE;

ANTIBODIES; CENTRIFUGATION, DENSITY GRADIENT; CHOLESTEROL; CYSTEINE ENDOPEPTIDASES; DETERGENTS; ERYTHROCYTE MEMBRANE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION; HOST-PARASITE INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE MICRODOMAINS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE ANNOTATION; PHOSPHOLIPIDS; PLASMODIUM FALCIPARUM; PROTEIN TRANSPORT; PROTEOME; PROTOZOAN PROTEINS; TROPHOZOITES;

EID: 84890615495     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.029272     Document Type: Article

References (52)

1. Maier, A. G., Cooke, B. M., Cowman, A. F., and Tilley, L. (2009) Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol 5, 341-354
2. de Koning-Ward, T. F., Gilson, P. R., Boddey, J. A., Rug, M., Smith, B. J., Papenfuss, A. T., Sanders, P. R., Lundie, R. J., Maier, A. G., Cowman, A. F., and Crabb, B. S. (2009) A newly discovered protein export machine in malaria parasites. Nature 7249, 945-949
3. Taraschi, T. F., Trelka, D., Martinez, S., Schneider, T., and 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. Int. J. Parasitol. 12, 1381-1391
4. Vincensini, L., Richert, S., Blisnick, T., Van Dorsselaer, A., Leize-Wagner, E., Rabilloud, T., and Braun Breton, C. (2005) Proteomic analysis identifies novel proteins of the Maurer's clefts, a secretory compartment delivering Plasmodium falciparum proteins to the surface of its host cell. Mol. Cell. Proteomics 4, 582-593
5. Wickham, M. E., Rug, M., Ralph, S. A., Klonis, N., McFadden, G. I., Tilley, L., and Cowman, A. F. (2001) Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes. EMBO J. 20, 5636-5649
6. Hanssen, E., Carlton, P., Deed, S., Klonis, N., Sedat, J., DeRisi, J., and Tilley, L. (2010) Whole cell imaging reveals novel modular features of the exomembrane system of the malaria parasite, Plasmodium falciparum. Int. J. Parasitol. 40, 123-134
7. Shevchenko, A., and Simons, K. (2010) Lipidomics: coming to grips with lipid diversity. Nat. Rev. Mol. Cell Biol. 11, 593-598
8. Goldston, A. M., Powell, R. R., and Temesvari, L. A. (2012) Sink or swim: lipid rafts in parasite pathogenesis. Trends Parasitol. 28, 417-426
9. Vieira, F. S., Corrêa, G., Einicker-Lamas, M., and Coutinho-Silva, R. (2010) Host-cell lipid rafts: a safe door for micro-organisms? Biol. Cell 102, 391-407
10. Simons, K., and Gerl, M. J. (2010) Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11, 688-699
11. Brown, D. A., and London, E. (2000) Structure and function of sphingolipidand cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224
12. Mañes, S., del Real, G., and Martínez, A. C. (2003) Pathogens: raft hijackers. Nat. Rev. Immunol. 3, 557-568
13. Murphy, S. C., Samuel, B. U., Harrison, T., Speicher, K. D., Speicher, D. W., Reid, M. E., Prohaska, R. Low, P. S., Tanner, M. J., Mohandas, N., and Haldar, K. (2004) Erythrocyte detergent-resistant membrane proteins: their characterization and selective uptake during malarial infection. Blood 103, 1920-1928
14. Murphy, S. C., Fernandez-Pol, S., Chung, P. H., Prasanna Murthy, S. N., Milne, S. B., Salomao, M., Brown, H. A., Lomasney, J. W., Mohandas, N., and Haldar, K. (2007) Cytoplasmic remodeling of erythrocyte raft lipids during infection by the human malaria parasite Plasmodium falciparum. Blood 110, 2132-2139
15. Labaied, M., Jayabalasingham, B., Bano, N., Cha, S. J., Sandoval, J., Guan, G., and Coppens, I. (2011) Plasmodium salvages cholesterol internalized by LDL and synthesized de novo in the liver. Cell. Microbiol. 13, 569-586
16. Sanders, P. R., Gilson, P. R., Cantin, G. T., Greenbaum, D. C., Nebl, T., Carucci, D. J., McConville, M. J., Schofield, L., Hodder, A. N., Yates, J. R., 3rd, and Crabb, B. S. (2005) Distinct protein classes including novel merozoite surface antigens in raft-like membranes of Plasmodium falciparum. J. Biol. Chem. 280, 40169-40176
17. Sanders, P. R., Cantin, G. T., Greenbaum, D. C., Gilson, P. R., Nebl, T., Moritz, R. L., Yates, J. R., 3rd, Hodder, A. N., and Crabb, B. S. (2007) Identification of protein complexes in detergent-resistant membranes of Plasmodium falciparum schizonts. Mol. Biochem. Parasitol. 154, 148-157
18. Di Girolamo, F., Raggi, C., Birago, C., Pizzi, E., Lalle, M., Picci, L., Pace, T., Bachi, A., de Jong, J., Janse, C. J., Waters, A. P., Sargiacomo, M., and Ponzi, M. (2008) Plasmodium lipid rafts contain proteins implicated in vesicular trafficking and signalling as well as members of the PIR superfamily, potentially implicated in host immune system interactions. Proteomics 8, 2500-2513
19. Trager, W., and Jensen, J. (1976) Human malaria parasites in continuous culture. Science 193, 673-675
20. López-Barragá n, M. J., Lemieux, J., Quiñones, M., Williamson, K. C., Molina-Cruz, A., Cui, K., Barillas-Mury, C., Zhao, K., and Su, X. Z. (2011) Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics 12, 587
21. Sargeant, T. J., Marti, M., Caler, E., Carlton, J. M., Simpson, K., Speed, T. P., and Cowman, A. F. (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol. 7, R12
22. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509
23. Frankland, S., Adisa, A., Horrocks, P., Taraschi, T. F., Schneider, T., Elliott, S. R., Rogerson, S. J., Knuepfer, E., Cowman, A. F., Newbold, C. I., and Tilley, L. (2006) Delivery of the malaria virulence protein PfEMP1 to the erythrocyte surface requires cholesterol-rich domains. Eukaryot. Cell 5, 849-860
24. van Dijk, M. R., van Schaijk, B. C., Khan, S. M., van Dooren, M. W., Ramesar, J., Kaczanowski, S., van Gemert, G. J., Kroeze, H., Stunnenberg, H. G., Eling, W. M., Sauerwein, R. W., Waters, A. P., and Janse, C. J. (2010) Three members of the 6-cys protein family of Plasmodium play a role in gamete fertility. PLoS Pathog. 6, e1000853
25. Banerjee, R., Liu, J., Beatty, W., Pelosof, L., Klemba, M., and Goldberg, D. E. (2002) Four plasmepsins are active in the Plasmodium falciparum food vacuole, including a protease with an active-site histidine. Proc. Natl. Acad. Sci. U.S.A. 99, 990-995
26. Hiller, N. L., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez- Estrano, C., and Haldar, K. (2004) Host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 5703, 1934-1937
27. Marti, M., Good, R. T., Rug, M., Knuepfer, E., and Cowman, A. F. (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 5703, 1930-1933
28. Salzer, U., and Prohaska, R. (2001) Stomatin, flotillin-1, and flotillin-2 are major integral proteins of erythrocyte lipid rafts. Blood 97, 1141-1143
29. 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., and Yates, J. R., 3rd. (2004) A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res. 14, 1052-1059
30. Salzer, U., Hinterdorfer, P., Hunger, U., Borken, C., and Prohaska, R. (2002) Ca(++)-dependent vesicle release from erythrocytes involves stomatinspecific lipid rafts, synexin (annexin 7), and sorcin. Blood 99, 2569-2577
31. Ciana, A., Balduini, C., and Minetti, G. (2005) Detergent-resistant membranes in human erythrocytes and their connection to the membraneskeleton. J. Biosci. 30, 317-328
32. Samuel, B. U., Mohandas, N., Harrison, T., McManus, H., Rosse, W., Reid, M., and Haldar, K. (2001) The role of cholesterol and glycosylphosphatidylinositol- anchored proteins of erythrocyte rafts in regulating raft protein content and malarial infection. J. Biol. Chem. 276, 29319-29329
33. Koshino, I., and Takakuwa, Y. (2009) Disruption of lipid rafts by lidocaine inhibits erythrocyte invasion by Plasmodium falciparum. Exp. Parasitol. 123, 381-383
34. Hiller, N. L., Akompong, T., Morrow, J. S., Holder, A. A., and Haldar, K. (2003) 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. 278, 48413-48421
35. Wang, L., Mohandas, N., Thomas, A., and Coppel, R. L. (2003) Detection of detergent-resistant membranes in asexual blood-stage parasites of Plasmodium falciparum. Mol. Biochem. Parasitol. 130, 149-153
36. Hoessli, D. C., Poincelet, M., Gupta, R., Ilangumaran, S., and Nasir-ud-Din (2003) Plasmodium falciparum merozoite surface protein 1. Eur. J. Biochem. 270, 366-375
37. Topolska, A. E., Lidgett, A., Truman, D., Fujioka, H., and Coppel, R. L. (2004) Characterization of a membrane-associated rhoptry protein of Plasmodium falciparum. J. Biol. Chem. 279, 4648-4656
38. Black, C. G., Wang, L., Topolska, A. E., Finkelstein, D. I., Horne, M. K., Thomas, A. W., Mohandas, N., and Coppel, R. L. (2004) Merozoite surface proteins 4 and 5 of Plasmodium knowlesi have differing cellular localisation and association with lipid rafts. Mol. Biochem. Parasitol. 138, 153-158
39. Proellocks, N. I., Kovacevic, S., Ferguson, D. J., Kats, L. M., Morahan, B. J., Black, C. G., Waller, K. L., and Coppel, R. L. (2007) Plasmodium falciparum Pf34, a novel GPI-anchored rhoptry protein found in detergentresistant microdomains. Int. J. Parasitol. 37, 1233-1241
40. Lauer, S., VanWye, J., Harrison, T., McManus, H., Samuel, B. U., Hiller, N. L., Mohandas, N., and Haldar, K. (2000) Vacuolar uptake of host components, and a role for cholesterol and sphingomyelin in malarial infection. EMBO J. 19, 3556-3564
41. Murphy, S. C., Hiller, N. L., Harrison, T., Lomasney, J. W., Mohandas, N., and Haldar K. (2006) Lipid rafts and malaria parasite infection of erythrocytes. Mol. Membr. Biol. 23, 81-88
42. Elias, J. E., Haas, W., Faherty, B. K., and Gygi, S. P. (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2, 667-675
43. Liu, J., Gluzman, I. Y., Drew, M. E., and Goldberg, D. E. (2005) The role of Plasmodium falciparum food vacuole plasmepsins. J. Biol. Chem. 280, 1432-1437
44. Klemba, M., Beatty, W., Gluzman, I., and Goldberg, D. E. (2004) Trafficking of plasmepsin 2 to the food vacuole of the malaria parasite Plasmodium falciparum. J. Cell Biol. 164, 47-56
45. Drew, M. E., Banerjee, R., Uffman, E. W., Gilbertson, S., Rosenthal, P. J., and Goldberg, D. E. (2008) Plasmodium food vacuole plasmepsins are activated by falcipains. J. Biol. Chem. 283, 12870-12876
46. Browman, D. T., Resek, M. E., Zajchowski, L. D., and Robbins, S. M. (2006) Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER. J. Cell Sci. 119, 3149-3160
47. Hayashi, T., and Fujimoto, M. (2010) Detergent-resistant microdomains determine the localization of sigma-1 receptors to the endoplasmic reticulum-mitochondria junction. Mol. Pharmacol. 77, 517-528
48. Ciarlo, L., Manganelli, V., Garofalo, T., Matarrese, P., Tinari, A., Misasi, R., Malorni, W., and Sorice, M. (2010) Association of fission proteins with mitochondrial raft-like domains. Cell Death Differ. 17, 1047-1058
49. van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008) Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124
50. Martin, R. E., Elliott, M. H., Brush, R. S., and Anderson, R. E. (2005) Detailed characterization of the lipid composition of detergent-resistant membranes from photoreceptor rod outer segment membranes. Invest. Ophthalmol. Vis. Sci. 46, 1147-1154
51. Sobo, K., Chevallier, J., Parton, R. G., Gruenberg, J., and van der Goot, F. G. (2007) Diversity of raft-like domains in late endosomes. PLoS One 2(4), e391
52. Proellocks, N. I., Kovacevic, S., Ferguson, D. J., Kats, L. M., Morahan, B. J., Black, C. G., Waller, K. L., and Coppel, R. L. (2007) Plasmodium falciparum Pf34, a novel GPI-anchored rhoptry protein found in detergentresistant microdomains. Int. J. Parasitol. 37, 1233-1241