Lipidomic analysis of Toxoplasma gondii tachyzoites rhoptries: Further insights into the role of cholesterol

Biochemical Journal

Volumn 415, Issue 1, 2008, Pages 86-96

  Besteiro, Sébastien ^a   Bertrand Michel, Justine ^b   Lebrun, Maryse ^a   Vial, Henri ^a   Dubremetz, Jean François ^a  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b INSERM   (France)

Author keywords

Cholesterol; Invasion; Lipidomic analysis; Raft; Rhoptry; Toxoplasma gondii

Indexed keywords

ACIDS; CELL MEMBRANES; CELLS; CYTOLOGY; FATTY ACIDS; LIPIDS;

INVASION; LIPIDOMIC ANALYSIS; RAFT; RHOPTRY; TOXOPLASMA GONDII;

CHOLESTEROL;

CHOLESTEROL; LIPID; SATURATED FATTY ACID; SPHINGOMYELIN; FATTY ACID;

ANISOTROPY; ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CELL SECRETION; CELL STRUCTURE; CONTROLLED STUDY; GAS LIQUID CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOST PARASITE INTERACTION; LIPIDOMICS; MEMBRANE FLUIDITY; NONHUMAN; PARASITE MIGRATION; PRIORITY JOURNAL; RHOPTRY; RIGIDITY; TACHYZOITE; TOXOPLASMA GONDII; ANIMAL; CHEMISTRY; FIBROBLAST; GAS CHROMATOGRAPHY; HUMAN; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; TOXOPLASMA; ULTRASTRUCTURE;

TOXOPLASMA; TOXOPLASMA GONDII;

ANIMALS; CHOLESTEROL; CHROMATOGRAPHY, GAS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FATTY ACIDS; FIBROBLASTS; HOST-PARASITE INTERACTIONS; HUMANS; LIPIDS; MEMBRANE FLUIDITY; MEMBRANE MICRODOMAINS; ORGANELLES; TOXOPLASMA;

EID: 53149122085     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20080795     Document Type: Article

References (49)

1. Oubremetz, J. F., Garcia-Reguet, N., Conseil, V. and Fourmaux, M. N. (1998) Apical organelles and host-cell invasion by Apicomplexa. Int. J. Parasitol. 28, 1007-1013
2. Bradley, P. J., Ward, C., Cheng, S. J., Alexander, D. L., Coller, S., Coombs, G. H., Dunn, J. D., Ferguson, D. J., Sanderson, S. J., Wastling, J. M. and Boothroyd, J. C. (2005) Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J. Biol. Chem. 280, 34245-34258
3. El Hajj, H., Lebrun, M., Arold, S. T., Vial, H., Labesse, G. and Dubremetz, J. F. (2007) ROP18 is a rhoptry kinase controlling the intracellular proliferation of Toxoplasma gondii. PLoS Pathog. 3, e14
4. Saeij, J. P., Boyle, J. P., Coller, S., Taylor, S., Sibley, L. D., Brooke-Powell, E. T., Ajioka, J. W. and Boothroyd, J. C. (2006) Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314, 1780-1783
5. Saeij, J. P., Coller, S., Boyle, J. P., Jerome, M. E., White, M. W. and Boothroyd, J. C. (2007) Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445, 324-327
6. Taylor, S., Barragan, A., Su, C., Fux, B., Fentress, S. J., Tang, K., Beatty, W. L., Hajj, H. E., Jerome, M., Behnke, M. S. et al. (2006) A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314, 1776-1780
7. Hakansson, S., Charron, A. J. and Sibley, L. D. (2001) Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole. EMBO J. 20, 3132-3144
8. Nichols, B. A., Chiappino, M. L. and O'Connor, G. R. (1983) Secretion from the rhoptries of Toxoplasma gondii during host-cell invasion. J. Ultrastruct. Res. 83, 85-98
9. Coppens, I. and Joiner. K. A. (2003) Host but not parasite cholesterol controls Toxoplasma cell entry by modulating organelle discharge. Mol. Biol. Cell 14, 3804-3820
10. Foussard, F., Leriche, M. A. and Dubremetz, J. F. (1991) Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitology 102, 367-370
11. Mordue, D. G., Desai, N., Dustin, M. and Sibley, L. D. (1999) Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring. J. Exp. Med. 190, 1783-1792
12. Charron, A. J. and Sibley, L. D. (2004) Molecular partitioning during host cell penetration by Toxoplasma gondii. Traffic 5, 855-867
13. Donald, R. G., Carter, D., Ullman, B. and Roos, D. S. (1996) Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J. Biol. Chem. 271, 14010-14019
14. Leriche, M. A. and Dulbremetz, J. F (1991) Characterization of the protein contents of rhoptries and dense granules of Toxoplasma gondii tachyzoites by subcellular fractionation and monoclonal antibodies. Mol. Biochem. Parasitol. 45, 249-259
15. El Hajj, H., Lebrun, M., Fourmaux, M. N., Vial, H. and Dubremetz, J. F. (2007) Inverted topology of the Toxoplasma gondii ROP5 rhoptry protein Provides new insights into the association of the ROP2 protein family with the parasitophorous vacuole membrane. Cell Microbiol. 9, 54-64
16. de Miguel, N., Echeverria, P. C. and Angel, S. O. (2005) Differential subcellular localization of members of the Toxoplasma gondii small heat shock protein family. Eukaryot. Cell 4, 1990-1997
17. Bermudes, D., Dubremetz. J. F., Achbarou, A. and Joiner, K. A. (1994) Cloning of a cDNA encoding the dense granule protein GRA3 from Toxoplasma gondii. Mol. Biochem. Parasitol. 68, 247-257
18. Couvreur, G., Sadak, A., Fortier, B. and Dubremetz, J. F. (1988) Surface antigens of Toxoplasma gondii. Parasitology 97, 1-10
19. Bligh, E. G. and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
20. Barrans, A., Collet, X., Barbaras, R., Jaspard, B., Manent, J., Vieu, C.. Chap, H. and Perret, B, (1994) Hepatic lipase induces the formation of pre-beta 1 high density lipoprotein (HDL) from triacylglycerol-rich HDL2. A study comparing liver perfusion to in vitro incubation with lipases. J. Biol. Chem. 269, 11572-11577
21. Vieu, C., Terce, F., Chevy, F., Rolland, C., Barbaras, R., Chap, H., Wolf, C., Perret, B. and Collet, X. (2002) Coupled assay of sphingomyelin and ceramide molecular species by gas liquid chromatography. J. Lipid Res. 43, 510-522
22. Lillington, J. M., Trafford, D. J. and Makin, H. L. (1981) A rapid and simple method for the esterification of fatty acids and steroid carboxylic acids prior to gas-liquid chromatography. Clin. Chim. Acta 111, 91-98
23. Shinitzky, M. and Barenholz, Y. (1978) Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta 515, 367-394
24. Blisnick, T., Morales Betoulle, M. E., Barale, J. C., Uzureau, P., Berry, L., Desroses, S., Fujioka, H., Mattei, D. and Braun, B. C. (2000) Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Mol. Biochem. Parasitol. 111, 107-121
25. Sadak, A., Taghy, Z., Fortier. B. and Dubremetz, J. F. (1988) Characterization of a family of rhoptry proteins of Toxoplasma gondii. Mol. Biochem. Parasitol. 29, 203-211
26. Ngo, H. M., Yang, M. and Joiner, K. A. (2004) Are rhoptries in Apicomplexan parasites secretory granules or secretory lysosomal granules? Mol. Microbiol. 52, 1531-1541
27. Welti, R., Mui, E., Sparks, A., Wernimont, S., Isaac, G., Kirisits, M., Roth, M., Roberts, C. W., Botte, C., Marechal, E. and McLeod, R. (2007) Lipidomic analysis of Toxoplasma gondii reveals unusual polar lipids. Biochemistry 46, 13882-13890
28. Mazumdar, J. and Striepen, B. (2007) Make it or take it: fatty acid metabolism of apicomplexan parasites. Eukaryot. Cell 6, 1727-1735
29. Gallois, Y., Foussard, F., Girault, A., Hodbert, J., Tricaud, A., Mauras, G. and Motta, C. (1988) Membrane fluidity of Toxoplasma gondii: a fluorescence polarization study. Biol. Cell 62, 11-15
30. Maxfield, F. R. and Tabas, I. (2005) Role of cholesterol and lipid organization in disease. Nature 438, 612-621
31. Nishikawa, Y., Quittnat, F., Stedman, T. T., Voelker, D. R., Choi, J. Y., Zahn, M., Yang, M., Pypaert, M., Joiner, K. A. and Coppens, I. (2005) Host cell lipids control cholesteryl ester synthesis and storage in intracellular Toxoplasma. Cell Microbiol. 7, 849-867
32. Athenstaedt, K. and Daum, G. (2006) The life cycle of neutral lipids: synthesis, storage and degradation. Cell. Mol. Life Sci. 63, 1355-1369
33. Zweytick, D., Athenstaedt, K. and Daum, G. (2000) Intracellular lipid particles of eukaryotic ceils. Biochim. Biophys. Acta 1469, 101-120
34. Coppens, I. and Vielemeyer, O. (2005) Insights into unique physiological features of neutral lipids in Apicomplexa: from storage to potential mediation in parasite metabolic activities. Int. J. Parasitol. 35, 597-615
35. Bloom. M., Evans, E. and Mouritsen, O. G. (1991) Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. O. Rev. Biophys. 24, 293-397
36. Stubbs, C. D. and Smith, A. D. (1984) The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim. Biophys. Acta 779, 89-137
37. Foussard, F., Gallois, Y., Girault, A. and Menez, J. F. (1991) Lipids and fatty acids of tachyzoites and purified pellicles of Toxoplasma gondii. Parasitol. Res. 77, 475-477
38. Chabanel, A., Flamm, M., Sung, K. L., Lee, M. M., Schachter, D. and Chien, S. (1983) Influence of cholesterol content on red cell membrane viscoelasticity and fluidity. Biophys. J. 44, 171-176
39. Mouritsen, O. G. and Zuckermann, M. J. (2004) What's so special about cholesterol? Lipids 39, 1101-1113
40. Oldfield, E. and Chapman, D. (1972) Dynamics of lipids in membranes: heterogeneity and the role of cholesterol. FEBS Lett. 23, 285-297
41. Manes, S., del Real, G. and Martinez, A. (2003) Pathogens: raft hijackers. Nat. Rev. Immunol. 3, 557-568
42. Wenk, M. R. (2006) Lipidomics of host-pathogen interactions. FEBS Lett. 580, 5541-5551
43. Lebrun, M., Michelin, A., El Hajj, H., Poncet, J., Bradley, P. J., Vial, H. and Dubremetz, J. F. (2005) The rhoptry neck protein RON4 re-localizes at the moving junction during Toxoplasma gondii invasion. Cell Microbiol. 7, 1823-1833
44. Maxfield, F. R. and Wustner, D. (2002) Intracellular cholesterol transport. J. Clin. Invest. 110, 891-898
45. 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. Memb, Biol. 23, 81-88
46. Albert, A. D. and Boesze-Battaglia, K. (2005) The role of cholesterol in rod outer segment membranes. Prog. Lipid Res. 44, 99-124
47. Orci, L., Montesano, R., Meda, P., Malaisse-Lagae, F., Brown, D., Perrelet, A. and Vassalli, P. (1981) Heterogeneous distribution of filipin-cholesterol complexes across the cisternae of the Golgi apparatus. Proc. Natl. Acad. Sci. U.S.A. 78, 293-297
48. Beckers, C. J., Dubremetz, J. F., Mercereau-Puijalon, O. and Joiner, K. A. (1994) The Toxoplasma gondii rhoptry protein ROP 2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. J. Cell Biol. 127, 947-961
49. Dodge, J. T. and Phillips, G. B. (1967) Composition of phospholipids and of phospholipid fatty acids and aldehydes in human red cells. J. Lipid Res. 8, 667-675