Conditional mutagenesis of a novel choline kinase demonstrates plasticity of phosphatidylcholine biogenesis and gene expression in Toxoplasma gondii

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16289-16299

  Sampels, Vera ^a   Hartmann, Anne ^a   Dietrich, Isabelle ^a   Coppens, Isabelle ^b   Sheiner, Lilach ^c   Striepen, Boris ^c   Herrmann, Andreas ^a   Lucius, Richard ^a   Gupta, Nishith ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE KINASE; CYTOSOLS; E. COLI; HYDROPHOBIC PEPTIDES; ISOFORMS; LIPID SYNTHESIS; N-TERMINALS; PARASITE-; PHOSPHATIDYLCHOLINE; PROTEIN LEVEL; PROTOZOAN PARASITES; TOXOPLASMA GONDII;

ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; MUTAGENESIS; OLIGOMERS; PLASTICITY;

BIOSYNTHESIS;

CHOLINE KINASE; DEANOL; GREEN FLUORESCENT PROTEIN; OLIGOMER; PHOSPHATIDYLCHOLINE;

ADAPTATION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CELL DIVISION; CELL MEMBRANE; CHOLINE KINASE GENE; CONDITIONAL MUTAGENESIS; CONTROLLED STUDY; CYTOSOL; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; ENZYME SYNTHESIS; EXON; GENE; GENE EXPRESSION; GENE LOSS; GENOME SIZE; HOST PARASITE INTERACTION; HYDROPHOBICITY; LIPOGENESIS; MICROBIAL GROWTH; MUTAGENESIS; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHOLIPID SYNTHESIS; PHOSPHORYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TOXOPLASMA GONDII;

BASE SEQUENCE; CHOLINE KINASE; DEANOL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; PHOSPHATIDYLCHOLINES; PROTEIN MULTIMERIZATION; PROTOZOAN PROTEINS; TOXOPLASMA;

PROTOZOA; TOXOPLASMA GONDII;

EID: 84860848421     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.347138     Document Type: Article

References (31)

1. Black, M. W., and Boothroyd, J. C. (2000) Lytic cycle of Toxoplasma gondii. Microbiol. Mol. Biol. Rev. 64, 607-623
2. Fox, B. A., and Bzik, D. J. (2002) De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature 415, 926-929 (Pubitemid 34174756)
3. Chaudhary, K., Darling, J. A., Fohl, L. M., Sullivan, W. J. Jr., Donald, R. G., Pfefferkorn, E. R., Ullman, B., and Roos, D. S. (2004) Purine salvage pathways in the apicomplexan parasite Toxoplasma gondii. J. Biol. Chem. 279, 31221-31227 (Pubitemid 39037787)
4. Blume, M., Rodriguez-Contreras, D., Landfear, S., Fleige, T., Soldati- Favre, D., Lucius, R., and Gupta, N. (2009) Host-derived glucose and its transporter in the obligate intracellular pathogen Toxoplasma gondii are dispensable by glutaminolysis. Proc. Natl. Acad. Sci. U.S.A. 106, 12998-13003
5. Welti, R., Mui, E., Sparks, A., Wernimont, S., Isaac, G., Kirisits, M., Roth, M., Roberts, C. W., Botté, C., Maréchal, E., and McLeod, R. (2007) Lipidomic analysis of Toxoplasma gondii reveals unusual polar lipids. Biochemistry 46, 13882-13890 (Pubitemid 350223915)
6. Maréchal, E., Azzouz, N., de Macedo, C. S., Block, M. A., Feagin, J. E., Schwarz, R. T., and Joyard, J. (2002) Synthesis of chloroplast galactolipids in apicomplexan parasites. Eukaryot. Cell 1, 653-656 (Pubitemid 36562391)
7. Gupta, N., Zahn, M. M., Coppens, I., Joiner, K. A., and Voelker, D. R. (2005) Selective disruption of phosphatidylcholine metabolism of the intracellular parasite Toxoplasma gondii arrests its growth. J. Biol. Chem. 280, 16345-16353 (Pubitemid 40616763)
8. Vance, J. E., and Vance, D. E. (2004) Phospholipid biosynthesis in mammalian cells. Biochem. Cell Biol. 82, 113-128 (Pubitemid 38580878)
9. Li, Z., Vance, D. E. (2008) Phosphatidylcholine and choline homeostasis. J. Lipid Res. 49, 1187-1194
10. Charron, A. J., and Sibley, L. D. (2002) Host cells: mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J. Cell Sci. 115, 3049-3059
11. Kim, K., Kim, K. H., Storey, M. K., Voelker, D. R., and Carman, G. (1999) Isolation and characterization of the Saccharomyces cerevisiae EKI1 gene encoding ethanolamine kinase. J. Biol. Chem. 274, 14857-14866
12. Porter, T. J., and Kent, C. (1992) Choline/ethanolamine kinase from rat liver. Methods Enzymol. 209, 134-146
13. Uchida, T., and Yamashita, S. (1992) Choline/ethanolamine kinase from rat brain. Methods Enzymol. 209, 147-153
14. 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
15. Donald, R. G., and Roos, D. S. (1993) Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug resistance mutations in malaria. Proc. Natl. Acad. Sci. U.S.A. 90, 11703-11707 (Pubitemid 24008707)
16. Fölsch, H., Pypaert, M., Schu, P., and Mellman, I. (2001) Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152, 595-606 (Pubitemid 34280241)
17. Meissner, M., Brecht, S., Bujard, H., and Soldati, D. (2001) Modulation of myosin A expression by a newly established tetracycline repressor-based inducible system in Toxoplasma gondii. Nucleic Acids Res. 29, E115
18. van Dooren, G. G., Tomova, C., Agrawal, S., Humbel, B. M., and Striepen, B. (2008) Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc. Natl. Acad. Sci. U.S.A. 105, 13574-13579
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. Sheiner, L., Demerly, J. L., Poulsen, N., Beatty, W. L., Lucas, O., Behnke, M. S., White, M. W., and Striepen, B. (2011) A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog. 7, e1002392
21. Rouser, G., Siakotos, A. N., and Fleischer, S. (1966) Quantitative analysis of phospholipids by thin layer chromatography and phosphorus analysis of spots. Lipids 1, 85-86
22. Witola, W. H., El Bissati, K., Pessi, G., Xie, C., Roepe, P. D., and Mamoun, C. B. (2008) Disruption of the Plasmodium falciparum PfPMT gene results in a complete loss of phosphatidylcholine biosynthesis via the serine-decarboxylase- phosphoethanolamine-methyltransferase pathway and severe growth and survival defects. J. Biol. Chem. 283, 27636-27643
23. Sinai, A. P., Webster, P., and Joiner, K. A. (1997) Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J. Cell Sci. 110, 2117-2128 (Pubitemid 27440435)
24. 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 (Pubitemid 30196707)
25. Goldstein, J. L., and Brown, M. S. (1977) The low-density lipoprotein pathway and its relation to atherosclerosis. Ann. Rev. Biochem. 46, 897-930
26. Mancuso, G., and Rugarli, E. I. (2008) A cryptic promoter in the first exon of the SPG4 gene directs the synthesis of the 60-kDa spastin isoform.BMC Biol. 6, 31
27. Alberge, B., Gannoun-Zaki, L., Bascunana, C., Tran van Ba, C., Vial, H., and Cerdan, R. (2010) Comparison of the cellular and biochemical properties of Plasmodium falciparum choline and ethanolamine kinases. Biochem. J. 425, 149-158
28. Gibellini, F., Hunter, W. N., and Smith, T. K. (2008) Biochemical characterization of the initial steps of the Kennedy pathway in Trypanosoma brucei: the ethanolamine and choline kinases. Biochem. J. 415, 135-144
29. Gallego-Ortega, D., Ramirez de Molina, A., Ramos, M. A., Valdes-Mora, F., Barderas, M. G., Sarmentero-Estrada, J., and Lacal, J. C. (2009) Differential role of human choline kinase α and β enzymes in lipid metabolism: implications in cancer onset and treatment. PLoS One 4, e7819
30. Kim, K. H., Voelker, D. R., Flocco, M. T., and Carman, G. M. (1998) Expression, purification, and characterization of choline kinase, product of the CKI gene from Saccharomyces cerevisiae. J. Biol. Chem. 273, 6844-6852 (Pubitemid 28160347)
31. Aoyama, C., Ohtani, A., and Ishidate, K. (2002) Expression and characterization of the active molecular forms of choline/ethanolamine kinase-α and -β in mouse tissues, including carbon tetrachloride-induced liver. Biochem. J. 363, 777-784 (Pubitemid 34526399)