Role of an ancestral D-bifunctional protein containing two sterol-carrier protein-2 domains in lipid uptake and trafficking in toxoplasma

Molecular Biology of the Cell

Volumn 20, Issue 2, 2009, Pages 658-672

  Lige, Bao ^a   Jayabalasingham, Bamini ^a   Zhang, Hui ^a   Pypaert, Marc ^b   Coppens, Isabelle ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COENZYME A; PHOSPHATIDYLCHOLINE; PROTOZOAL PROTEIN; STEROL CARRIER PROTEIN 2; CARRIER PROTEIN; CHOLESTEROL; HSD17B4 PROTEIN, HUMAN; HYBRID PROTEIN; HYDROLYASE; HYDROXYSTEROID DEHYDROGENASE; MEMBRANE LIPID; STEROL; STEROL CARRIER PROTEINS;

ANIMAL CELL; ARTICLE; CELL ORGANELLE; CELL TRANSPORT; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID METABOLISM; LIPID TRANSPORT; MAMMAL CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; TOXOPLASMA; TOXOPLASMA GONDII; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN PROCESSING; SEQUENCE ALIGNMENT; TRANSPORT AT THE CELLULAR LEVEL; ZELLWEGER SYNDROME;

EUKARYOTA; MAMMALIA; PROTOZOA; TOXOPLASMA;

17-HYDROXYSTEROID DEHYDROGENASES; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL LINE; CHOLESTEROL; HUMANS; HYDRO-LYASES; LIPID METABOLISM; MEMBRANE LIPIDS; MOLECULAR SEQUENCE DATA; PEROXISOMES; PHOSPHATIDYLCHOLINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; STEROLS; TOXOPLASMA; ZELLWEGER SYNDROME;

EID: 61949285138     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-05-0482     Document Type: Article

References (40)

1. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
2. Atshaves, B. P., Storey, S. M., McIntosh, A. L., Petrescu, A. D., Lyuksyutova, O. I., Greenberg, A. S., and Schroeder, F. (2001). Sterol carrier protein-2 expression modulates protein and lipid composition of lipid droplets. J. Biol. Chem. 276, 25324-25335.
3. Atshaves, B. P., Gallegos, A. M., Mcintosh, A. L., Kier, A. B., and Schroeder, F. (2003). Sterol carrier protein-2 selectively alters lipid composition and cholesterol dynamics of caveolae/lipid raft vs nonraft domains in L-cell fibroblast plasma membranes. Biochemistry 42, 14583-14598.
4. Avdulov, N. A., Chochina, S. V., Igbavboa, U., Warden, C. S., Schroeder, F., and Wood, W. G. (1999). Lipid binding to sterol carrier protein-2 is inhibited by ethanol. Biochim. Biophys. Acta 1437, 37-45.
5. Bradley, P. J., et al. (2005). Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii. J. Biol. Chem. 280, 34245-34258.
6. Brasaemle, D. L., and Attie, A. D. (1990). Rapid intracellular transport of LDL-derived cholesterol to the plasma membrane in cultured fibroblasts. J. Lipid Res. 31, 103-112.
7. Choinowski, T., Hauser, H., and Piontek, K. (2000). Structure of sterol carrier protein 2 at 1.8 A resolution reveals a hydrophobic tunnel suitable for lipid binding. Biochemistry 39, 1897-1902.
8. Coppens, I., Levade, T., and Courtoy, P. J. (1995). Host plasma low density lipoprotein particles as an essential source of lipids for the bloodstream forms of Trypanosoma brucei. J. Biol. Chem. 270, 5736-5741.
9. Coppens, I., Sinai, A. P., and Joiner, K. A. (2000). Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J. Cell Biol. 149, 167-180.
10. 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.
11. Coppens, I. (2006). Contribution of host lipids to Toxoplasma pathogenesis. Cell. Microbiol. 8, 1-9.
12. Ding, M., Clayton, C., and Soldati, D. (2000). Toxoplasma gondii catalase: are there peroxisomes in Toxoplasma? J. Cell Sci. 113, 2409-2419.
13. Ding, M., Kwok, L. Y., Schluter, D., Clayton, C., and Soldati, D. (2004). The antioxidant systems in Toxoplasma gondii and the role of cytosolic catalase in defence against oxidative injury. Mol. Microbiol. 51, 47-61.
14. Dodt, G., and Gould, S. J. (1996). Multiple PEX genes are required for proper subcellular distribution and stability of Pex5p, the PTS1 receptor: evidence that PTS1 protein import is mediated by a cycling receptor. J. Cell Biol. 135, 1763-1774.
15. Dyer, D. H., Lovell, S., Thoden, J. B., Holden, H. M., Rayment, I., and Lan, Q. (2003). The structural determination of an insect sterol carrier protein-2 with a ligand-bound C16 fatty acid at 1.35-A resolution. J. Biol. Chem. 278, 39085-39091.
16. Edqvist, J., Rönnberg, E., Rosenquist, S., Blomqvist, K., Viitanen, L., Salminen, T. A., Nylund, M., Tuuf, J., and Mattjus, P. (2004). Plants express a lipid transfer protein with high similarity to mammalian sterol carrier protein-2. J. Biol. Chem. 279, 53544-53553.
17. Edqvist, J., and Blomqvist, K. (2006). Fusion and fission, the evolution of sterol carrier protein-2. J. Mol. Evol. 62, 292-306.
18. Gallegos, A. M., Atshaves, B. P., Storey, S. M., Starodub, O., Petrescu, A. D., Huang, H., McIntosh, A. L., Martin, G. G., Chao, H., et al. (2001). Gene structure, intracellular localization, and functional roles of sterol carrier protein-2. Prog. Lipid Res. 40, 498-563.
19. Gould, S. J., Keller, G. A., Hosken, N., Wilkinson, J., and Subramani, S. (1989). A conserved tripeptide sorts proteins to peroxisomes. J. Cell Biol. 108, 1657-1664.
20. Gubbles, M. J., Vaishnava, S., Boot, N., Dubremetz, J. F., and Striepen, B. (2006). A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J. Cell Sci. 119, 2236-2245.
21. Hu, K. (2008). Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii. PLoS Pathog. 4, e10.
22. Kaasch, A. J., and Joiner, K. A. (2000). Targeting and subcellular localization of Toxoplasma gondii catalase. Identification of peroxisomes in an apicomplexan parasite. J. Biol. Chem. 275, 1112-1118.
23. Keller, G. A., Krisans, S., Gould, S. J., Sommer, J. M., Wang, C. C., Schliebs, W., Kunau, W., Brody, S., and Subramani, S. (1991). Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes, and glycosomes. J. Cell Biol. 114, 893-904.
24. Mattjus, P., Molotkovsky, J. G., Smaby, J. M., and Brown, R. E. (1999). A fluorescence resonance energy transfer approach for monitoring protein-mediated glycolipid transfer between vesicle membranes. Anal. Biochem. 268, 297-304.
25. Moncecchi, D., Murphy, E. J., Prows, D. R., and Schroeder, F. (1996). Sterol carrier protein-2 expression in mouse L-cell fibroblasts alters cholesterol uptake. Biochim. Biophys. Acta 1302, 110-116.
26. Mukherji, M., Kershaw, N. J., Schofield, C. J., Wierzbicki, A. S., and Lloyd, M. D. (2002). Utilization of sterol carrier protein-2 by phytanoyl-CoA 2-hydroxylase in the peroxisomal α oxidation of phytanic acid. Chem. Biol. 9, 597-605.
27. Murphy, E. J. (2002). Sterol carrier protein-2, not just for cholesterol any more. Mol. Cell. Biochem. 239, 87-93.
28. Neuberger, G., Kunze, M., Eisenhaber, F., Berger, J., Hartig, A., and Brocard, C. (2004). Hidden localization motifs: naturally occurring peroxisomal targeting signals in non-peroxisomal proteins. Genome Biol. 5, R97.
29. 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.
30. Prinz, W. A. (2007). Non-vesicular sterol transport in cells. Prog. Lipid Res. 46, 297-314.
31. Puglielli, L., Rigotti, A., Greco, A. V., Santos, M. J., and Nervi, F. (1995). Sterol carrier protein-2 is involved in cholesterol transfer from the endoplasmic reticulum to the plasma membrane in human fibroblasts. J. Biol. Chem. 270, 18723-18726.
32. Quittnat, F. et al. (2004). On the biogenesis of lipid bodies in ancient eukaryotes: synthesis of triacylglycerols by a Toxoplasma DGAT1-related enzyme. Mol. Biochem. Parasitol. 138, 107-122.
33. Raychaudhuri, S., Im, Y. J., Hurley, J. H., and Prinz, W. A. (2006). Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J. Cell Biol. 173, 107-119.
34. Roos, D. S., Donald, R. G., Morrissette, N. S., and Moulton, A. L. (1994). Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45, 27-63.
35. Sehgal, A., Bettiol, S., Pypaert, M., Wenk, M. R., Kaasch, A., Blader, I. J., Joiner, K. A., and Coppens, I. (2005). Peculiarities of host cholesterol transport to the unique intracellular vacuole containing Toxoplasma. Traffic 6, 1125-1141.
36. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985). Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85.
37. Stolowich, N. J., Petrescu, A. D., Huang, H., Martin, G. G., Scott, A. I., and Schroeder, F. (2002). Sterol carrier protein-2, structure reveals function. Cell. Mol. Life Sci. 59, 193-212.
38. Titorenko, V. I., and Rachubinski, R. A. (2001). The life cycle of the peroxisome. Nat. Rev. Mol. Cell Biol. 2, 357-368.
39. Wenk, M. R. (2006). Lipidomics of host-pathogen interactions. FEBS Lett. 580, 5541-5551.
40. Zhou, M., Parr, R. D., Petrescu, A. D., Payne, H. R., Atshaves, B. P., Kier, A. B., Ball, J. M., and Schroeder, F. (2004). Sterol carrier protein-2 directly interacts with caveolin-1 in vitro and in vivo. Biochemistry 43, 7288-7306.