A novel protein kinase localized to lipid droplets is required for droplet biogenesis in trypanosomes

Eukaryotic Cell

Volumn 9, Issue 11, 2010, Pages 1702-1710

  Flaspohler, John A ^a,b   Jensen, Bryan C ^a   Saveria, Tracy ^a   Kifer, Charles T ^a   Parsons, Marilyn ^a,c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b and Exercise Science   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE; PROTOZOAL DNA; PROTOZOAL PROTEIN;

ARTICLE; CELL ORGANELLE; DRUG ANTAGONISM; GENE; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; NUCLEOTIDE SEQUENCE; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

BASE SEQUENCE; DNA, PROTOZOAN; GENE KNOCKDOWN TECHNIQUES; GENES, PROTOZOAN; LIPID METABOLISM; ORGANELLES; PROTEIN KINASES; PROTOZOAN PROTEINS; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; HEXAPODA; MAMMALIA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 78149243021     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00106-10     Document Type: Article

References (53)

1. Alibu, V. P., L. Storm, S. Haile, C. Clayton, and D. Horn. 2005. A doubly inducible system for RNA interference and rapid RNAi plasmid construction in Trypanosoma brucei. Mol. Biochem. Parasitol. 139:75-82.
2. Allen, C. L., D. Goulding, and M. C. Field. 2003. Clathrin-mediated endo- cytosis is essential in Trypanosoma brucei. EMBO J. 22:4991-5002.
3. Athenstaedt, K., D. Zweytick, A. Jandrositz, S. D. Kohlwein, and G. Daum. 1999. Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J. Bacteriol. 181:6441-6448.
4. Bangs, J. D., L. Uyetake, M. J. Brickman, A. E. Balber, and J. C. Boothroyd. 1993. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei: divergent ER retention signals in a lower eukaryote. J. Cell Sci. 105:1101-1113.
5. Beller, M., D. Riedel, L. Jansch, G. Dieterich, J. Wehland, H. Jackle, and R. P. Kuhnlein. 2006. Characterization of the Drosophila lipid droplet sub- proteome. Mol. Cell. Proteomics 5:1082-1094.
6. Beller, M., C. Sztalryd, N. Southall, M. Bell, H. Jackle, D. S. Auld, and B. Oliver. 2008. COPI complex is a regulator of lipid homeostasis. PLoS Biol. 6:e292.
7. Besteiro, S., M. P. Barrett, L. Riviere, and F. Bringaud. 2005. Energy gen- eration in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol. 21:185-191.
8. Blanchette-Mackie, E. J., N. K. Dwyer, T. Barber, R. A. Coxey, T. Takeda, C. M. Rondinone, J. L. Theodorakis, A. S. Greenberg, and C. Londos. 1995. Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36:1211-1226.
9. Bordier, C. 1981. Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256:1604-1607.
10. Bougneres, L., J. Helft, S. Tiwari, P. Vargas, B. H. Chang, L. Chan, L. Campisi, G. Lauvau, S. Hugues, P. Kumar, A. O. Kamphorst, A. M. Dume- nil, M. Nussenzweig, J. D. MacMicking, S. Amigorena, and P. Guermonprez. 2009. A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31:232-244.
11. Brasaemle, D. L., G. Dolios, L. Shapiro, and R. Wang. 2004. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279:46835-46842.
12. Cermelli, S., Y. Guo, S. P. Gross, and M. A. Welte. 2006. The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr. Biol. 16: 1783-1795.
13. Cornell, R. B., and S. G. Taneva. 2006. Amphipathic helices as mediators of the membrane interaction of amphitropic proteins, and as modulators of bilayer physical properties. Curr. Protein Peptide Sci. 7:539-552.
14. Cox, J. S., C. E. Shamu, and P. Walter. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a trans- membrane protein kinase. Cell 73:1197-1206.
15. Das, A., J.-H. Park, C. B. Hagen, and M. Parsons. 1998. Distinct domains of a nucleolar protein mediate protein kinase binding, interaction with nucleic acids and nucleolar localization. J. Cell Sci. 111:2615-2623.
16. El-Sayed, N. M., P. J. Myler, D. C. Bartholomeu, D. Nilsson, G. Aggarwal, A. N. Tran, E. Ghedin, E. A. Worthey, A. L. Delcher, G. Blandin, S. J. Westenberger, E. Caler, G. C. Cerqueira, C. Branche, B. Haas, A. Anupama, E. Arner, L. Aslund, P. Attipoe, E. Bontempi, F. Bringaud, P. Burton, E. Cadag, D. A. Campbell, M. Carrington, J. Crabtree, H. Darban, J. F. Da Silveira, P. de Jong, K. Edwards, P. T. Englund, G. Fazelina, T. Feldblyum, M. Ferella, A. C. Frasch, K. Gull, D. Horn, L. Hou, Y. Huang, E. Kindlund, M. Klingbeil, S. Kluge, H. Koo, D. Lacerda, M. J. Levin, H. Lorenzi, T. Louie, C. R. Machado, R. McCulloch, A. McKenna, Y. Mizuno, J. C. Mot- tram, S. Nelson, S. Ochaya, K. Osoegawa, G. Pai, M. Parsons, M. Pentony, U. Pettersson, M. Pop, J. L. Ramirez, J. Rinta, L. Robertson, S. L. Salzberg, D. O. Sanchez, A. Seyler, R. Sharma, J. Shetty, A. J. Simpson, E. Sisk, M. T. Tammi, R. Tarleton, S. Teixeira, S. Van Aken, C. Vogt, P. N. Ward, B. Wickstead, J. Wortman, O. White, C. M. Fraser, K. D. Stuart, and B. Andersson. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415.
17. Fang, J., P. Rohloff, K. Miranda, and R. Docampo. 2007. Ablation of a small transmembrane protein of Trypanosoma brucei (TbVTC1) involved in the synthesis of polyphosphate alters acidocalcisome biogenesis and function, and leads to a cytokinesis defect. Biochem. J. 407:161-170.
18. Farese, R. V., Jr., and T. C. Walther. 2009. Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139:855-860.
19. Field, M. C., and M. Carrington. 2004. Intracellular membrane transport systems in Trypanosoma brucei. Traffic 5:905-913.
20. Fridberg, A., C. L. Olson, E. S. Nakayasu, K. M. Tyler, I. C. Almeida, and D. M. Engman. 2008. Sphingolipid synthesis is necessary for kinetoplast segregation and cytokinesis in Trypanosoma brucei. J. Cell Sci. 121:522-535.
21. Friesen, J. A., H. A. Campbell, and C. Kent. 1999. Enzymatic and cellular characterization of a catalytic fragment of CTP: phosphocholine cytidylyltransferase alpha. J. Biol. Chem. 274:13384-13389.
22. Fujiki, Y., A. L. Hubbard, S. Fowler, and P. B. Lazarow. 1982. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 61:97-102.
23. Fujimoto, Y., H. Itabe, J. Sakai, M. Makita, J. Noda, M. Mori, Y. Higashi, S. Kojima, and T. Takano. 2004. Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim. Biophys. Acta 1644:47-59.
24. Fukumoto, S., and T. Fujimoto. 2002. Deformation of lipid droplets in fixed samples. Histochem. Cell Biol. 118:423-428.
25. Guo, Y., C. Walther, M. Rao, N. Stuurman, G. Goshima, K. Terayama, J. S. Wong, R. D. Vale, P. Walter, and R. V. Farese. 2008. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453:657-661.
26. Hanks, S. K., and T. Hunter. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
27. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
28. Ikeda, M., Y. Kida, S. Ikushiro, and M. Sakaguchi. 2005. Manipulation of membrane protein topology on the endoplasmic reticulum by a specific ligand in living cells. J. Biochem. 138:631-637.
29. Ingelmo-Torres, M., E. Gonzalez-Moreno, A. Kassan, M. Hanzal-Bayer, F. Tebar, A. Herms, T. Grewal, J. F. Hancock, C. Enrich, M. Bosch, S. P. Gross, R. G. Parton, and A. Pol. 2009. Hydrophobic and basic domains target proteins to lipid droplets. Traffic 10:1785-1801.
30. Jensen, B. C., D. L. Brekken, A. C. Randall, C. T. Kifer, and M. Parsons. 2005. Species specificity in ribosome biogenesis: a nonconserved phosphoprotein is required for formation of the large ribosomal subunit in Trypanosoma brucei. Eukaryot. Cell 4:30-35.
31. Jensen, B. C., D. Sivam, C. T. Kifer, P. J. Myler, and M. Parsons. 2009. Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10:482.
32. Jensen, B. C., Q. Wang, C. T. Kifer, and M. Parsons. 2003. The NOG1 GTP-binding protein is required for biogenesis of the 60S ribosomal subunit. J. Biol. Chem. 278:32204-32211.
33. Kamisaka, Y., N. Noda, and M. Yamaoka. 2004. Appearance of smaller lipid bodies and protein kinase activation in the lipid body fraction are induced by an increase in the nitrogen source in the Mortierella fungus. J. Biochem. 135:269-276.
34. Lee, S. H., J. L. Stephens, K. S. Paul, and P. T. Englund. 2006. Fatty acid synthesis by elongases in trypanosomes. Cell 126:691-699.
35. Lemercier, G., S. Dutoya, S. Luo, F. A. Ruiz, C. O. Rodrigues, T. Baltz, R. Docampo, and N. Bakalara. 2002. A vacuolar-type H -pyrophosphatase governs maintenance of functional acidocalcisomes and growth of the insect and mammalian forms of Trypanosoma brucei. J. Biol. Chem. 277:37369-37376.
36. Listenberger, L. L., and D. A. Brown. 2007. Fluorescent detection of lipid droplets and associated proteins. Curr. Protoc. Cell Biol. Chapter 24:Unit 24.2.
37. Liu, P., Y. Ying, Y. Zhao, D. I. Mundy, M. Zhu, and R. G. Anderson. 2004. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279:3787-3792.
38. Moraes, M. C., T. C. Jesus, N. N. Hashimoto, M. Dey, K. J. Schwartz, V. S. Alves, C. C. Avila, J. D. Bangs, T. E. Dever, S. Schenkman, and B. A. Castilho. 2007. A novel membrane-bound eIF2 alpha kinase in the flagellar pocket of Trypanosoma brucei. Eukaryot. Cell 6:1979-1991.
39. Morita, Y. S., K. S. Paul, and P. T. Englund. 2000. Specialized fatty acid synthesis in African trypanosomes: myristate for GPI anchors. Science 288: 140-143.
40. Murphy, D. J. 2001. The biogenesis and functions of lipid bodies in animals, plants, and microorganisms. Prog. Lipid Res. 40:325-438.
41. Ozeki, S., J. Cheng, K. Tauchi-Sato, N. Hatano, H. Taniguchi, and T. Fuji- moto. 2005. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J. Cell Sci. 118: 2601-2611.
42. Park, J. H., D. L. Brekken, A. C. Randall, and M. Parsons. 2002. Molecular cloning of Trypanosoma brucei CK2 catalytic subunits: the alpha isoform is nucleolar and phosphorylates the nucleolar protein Nopp44/46. Mol. Biochem. Parasitol. 119:97-106.
43. Parker, H. L., T. Hill, K. Alexander, N. B. Murphy, W. R. Fish, and M. Parsons. 1995. Three genes and two isozymes: gene conversion and the compartmentalization and expression of the phosphoglycerate kinases of Trypanosoma (Nannomonas) congolense. Mol. Biochem. Parasitol. 69:269-279.
44. Parsons, M., E. A. Worthey, P. N. Ward, and J. C. Mottram. 2005. Com- parative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei, and Trypanosoma cruzi. BMC Genomics 6:127.
45. Richardson, J. P., R. P. Beecroft, D. L. Tolson, M. K. Liu, and T. W. Pearson. 1988. Procyclin: an unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes. Mol. Biochem. Parasitol. 31:203-216.
46. Shalaby, T., M. Liniger, and T. Seebeck. 2001. The regulatory subunit of a cGMP-regulated protein kinase A of Trypanosoma brucei. Eur. J. Biochem. 268:6197-6206.
47. Sutterwala, S. S., F. F. Hsu, E. S. Sevova, K. J. Schwartz, K. Zhang, P. Key, J. Turk, S. M. Beverley, and J. D. Bangs. 2008. Developmentally regulated sphingolipid synthesis in African trypanosomes. Mol. Microbiol. 70:281-296.
48. Tauchi-Sato, K., S. Ozeki, T. Houjou, R. Taguchi, and T. Fujimoto. 2002. The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J. Biol. Chem. 277:44507-44512.
49. Van Hellemond, J. J., and A. G. Tielens. 2006. Adaptations in the lipid metabolism of the protozoan parasite Trypanosoma brucei. FEBS Lett. 580:5552-5558.
50. van Herpen, R. E., R. J. Oude Ophuis, M. Wijers, M. B. Bennink, F. A. van de Loo, J. Fransen, B. Wieringa, and D. G. Wansink. 2005. Divergent mitochondrial and endoplasmic reticulum association of DMPK splice isoforms depends on unique sequence arrangements in tail anchors. Mol. Cell. Biol. 25:1402-1414.
51. Vickerman, K. 1985. Developmental cycles and biology of pathogenic try- panosomes. Br. Med. Bull. 41:105-114.
52. Wirtz, E., S. Leal, C. Ochatt, and G. A. Cross. 1999. A tightly regulated inducible expression system for conditional gene knockouts and dominantnegative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89101.
53. Yu, W., P. T. Bozza, D. M. Tzizik, J. P. Gray, J. Cassara, A. M. Dvorak, and P. F. Weller. 1998. Co-compartmentalization of MAP kinases and cytosolic phospholipase A2 at cytoplasmic arachidonate-rich lipid bodies. Am. J. Pathol. 152:759-769.