The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy

Molecular and Cellular Proteomics

Volumn 4, Issue 5, 2005, Pages 662-672

  Natter, Klaus ^a   Leitner, Peter ^a   Faschinger, Alexander ^a   Wolinski, Heimo ^a   McCraith, Stephen ^b,c   Fields, Stanley ^b   Kohlwein, Sepp D ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Bothel Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LIPID; SACCHAROMYCES CEREVISIAE PROTEIN; SPHINGOLIPID; STEROL;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL MEMBRANE; CELL NUCLEUS; CELL VACUOLE; CELLULAR DISTRIBUTION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME LOCALIZATION; GENE INTERACTION; GOLGI COMPLEX; LIPID METABOLISM; LIPOGENESIS; METABOLIC REGULATION; MITOCHONDRION; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STEROL METABOLISM;

BIOLOGICAL MARKERS; ENDOPLASMIC RETICULUM; GREEN FLUORESCENT PROTEINS; LIPID METABOLISM; MICROSCOPY, CONFOCAL; MITOCHONDRIA; PEROXISOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBCELLULAR FRACTIONS;

SACCHAROMYCES CEREVISIAE;

EID: 18944406929     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M400123-MCP200     Document Type: Article

References (55)

1. Tuller, G., Nemec, T., Hrastnik, C. & Daum, G. (1999) Lipid composition of subcellular membranes of an FY1679-derived haploid yeast wild-type strain grown on different carbon sources. Yeast 15, 1555-1564
2. Brugger, B., Erben, G., Sandhoff, R., Wieland, F. T. & Lehmann, W. D. (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 94, 2339-2344
3. Schneiter, R., Brugger, B., Sandhoff, R., Zellnig, G., Leber, A., Lampl, M., Athenstaedt, K., Hrastnik, C., Eder, S., Daum, G., Paltauf, F., Wieland, F. T. & Kohlwein, S. D. (1999) Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J. Cell. Biol. 146, 741-754
4. Achleitner, G., Gaigg, B., Krasser, A., Kainersdorfer, E., Kohlwein, S. D., Perktold, A., Zellnig, G. & Daum, G. (1999) Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact. Eur. J. Biochem. 264, 545-553
5. Pichler, H., Gaigg, B., Hrastnik, C., Achleitner, G., Kohlwein, S. D., Zellnig, G., Perktold, A. & Daum, G. (2001) A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur. J. Biochem. 268, 2351-2361
6. Wagner, S. & Paltauf, F. (1994) Generation of glycerophospholipid molecular species in the yeast Saccharomyces cerevisiae. Fatty acid pattern of phospholipid classes and selective acyl turnover at sn-1 and sn-2 positions. Yeast 10, 1429-1437
7. Kumar, A., Agarwal, S., Heyman, J. A., Matson, S., Heidtman, M., Piccirillo, S., Umansky, L., Drawid, A., Jansen, R., Liu, Y., Cheung, K. H., Miller, P., Gerstein, M., Roeder, G. S. & Snyder, M. (2002) Subcellular localization of the yeast proteome. Genes Dev. 16, 707-719
8. Tatchell, K. & Robinson, L. C. (2002) Use of green fluorescent protein in living yeast cells. Methods Enzymol. 351, 661-683
9. Kohlwein, S. D. (2000) The beauty of the yeast: live cell microscopy at the limits of optical resolution. Microsc. Res. Tech. 51, 511-529
10. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. & O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691
11. Hazbun, T. R., Malmstrom, L., Anderson, S., Graczyk, B. J., Fox, B., Riffle, M., Sundin, B. A., Aranda, J. D., McDonald, W. H., Chiu, C. H., Snydsman, B. E., Bradley, P., Muller, E. G., Fields, S., Baker, D., Yates, J. R., III & Davis, T. N. (2003). Assigning function to yeast proteins by integration of technologies. Mol. Cell 12, 1353-1365
12. Zhu, H., Klemic, J. F., Chang, S., Bertone, P., Casamayor, A., Klemic, K. G., Smith, D., Gerstein, M., Reed, M. A. & Snyder, M. (2000) Analysis of yeast protein kinases using protein chips. Nat. Genet. 26, 283-289
13. Hudson, J. R., Jr., Dawson, E. P., Rushing, K. L., Jackson, C. H., Lockshon, D., Conover, D., Lanciault, C., Harris, J. R., Simmons, S. J., Rothstein, R. & Fields, S. (1997) The complete set of predicted genes from Saccharomyces cerevisiae in a readily usable form. Genome Res. 7, 1169-1173
14. Ma, H., Kunes, S., Schatz, P. J. & Botstein, D. (1987) Plasmid construction by homologous recombination in yeast. Gene (Amst.) 58, 201-216
15. Uetz, P., Giot, L., Cagney, G., Mansfield, T. A., Judson, R. S., Knight, J. R., Lockshon, D., Narayan, V., Srinivasan, M., Pochart, P., Qureshi-Emili, A., Li, Y., Godwin, B., Conover, D., Kalbfleisch, T., Vijayadamodar, G., Yang, M., Johnston, M., Fields, S. & Rothberg, J. M. (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403, 623-627
16. Kals, M., Natter, K., Thallinger, G. G., Trajanoski, Z. & Kohlwein, S. D. (2005) YPL.db2: the Yeast Protein Localization database, version 2.0. Yeast 22, 213-218
17. Habeler, G., Natter, K., Thallinger, G. G., Crawford, M. E., Kohlwein, S. D. & Trajanoski, Z. (2002) YPL.db: the Yeast Protein Localization database. Nucleic Acids Res. 30, 80-83
18. Christie, K. R., Weng, S., Balakrishnan, R., Costanzo, M. C., Dolinski, K., Dwight, S. S., Engel, S. R., Feierbach, B., Fisk, D. G., Hirschman, J. E., Hong, E. L., Issel-Tarver, L., Nash, R., Sethuraman, A., Starr, B., Theesfeld, C. L., Andrada, R., Binkley, G., Dong, Q., Lane, C., Schroeder, M., Botstein, D. & Cherry, J. M. (2004) Saccharomyces Genome Database (SGD) provides tools to identify and analyze sequences from Saccharomyces cerevisiae and related sequences from other organisms. Nucleic Acids Res 32, D311-D314
19. Mumberg, D., Muller, R. & Funk, M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene (Amst.) 156, 119-122
20. Ito, H., Fukuda, Y., Murata, K. & Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168
21. Horvath, A. & Riezman, H. (1994) Rapid protein extraction from Saccharomyces cerevisiae. Yeast 10, 1305-1310
22. Mewes, H. W., Amid, C., Arnold, R., Frishman, D., Guldener, U., Mannhaupt, G., Munsterkotter, M., Pagel, P., Strack, N., Stumpflen, V., Warfsmann, J. & Ruepp, A. (2004). MIPS: analysis and annotation of proteins from whole genomes. Nucleic Acids Res. 32, D41-D44
23. Cagney, G., Uetz, P. & Fields, S. (2000) High-throughput screening for protein-protein interactions using two-hybrid assay. Methods Enzymol. 328, 3-14
24. Caro, L. H., Tettelin, H., Vossen, J. H., Ram, A. F., van den Ende, H. & Klis, F. M. (1997) In silico identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces carevisiae. Yeast 13, 1477-1489
25. Simpson, J. C., Wellenreuther, R., Poustka, A., Pepperkok, R. & Wiemann, S. (2000) Systematic subcellular localization of novel proteins identified by large-scale cDNA sequencing. EMBO Rep. 1, 287-292
26. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M. & Sherlock, G. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29
27. Swedlow, J. R., Goldberg, I., Brauner, E. & Sorger, P. K. (2003) Informatics and quantitative analysis in biological imaging. Science 300, 100-102
28. Hampton, R. Y. (2002) Proteolysis and sterol regulation. Annu. Rev. Cell Dev. Biol. 18, 345-378
29. Milla, P., Athenstaedt, K., Viola, F., Oliaro-Bosso, S., Kohlwein, S. D., Daum, G. & Balliano, G. (2002) Yeast oxidosqualene cyclase (Erg7p) is a major component of lipid particles. J. Biol. Chem. 277, 2406-2412
30. Leber, R., Landl, K., Zinser, E., Ahorn, H., Spok, A., Kohlwein, S. D., Turnowsky, F. & Daum, G. (1998) Dual localization of squalene epoxidase, Erg1p, in yeast reflects a relationship between the endoplasmic reticulum and lipid particles. Mol. Biol. Cell 9, 375-386
31. Athenstaedt, K., Zweytick, D., Jandrositz, A., Kohlwein, S. D. & Daum, G. (1999) Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J. Bacteriol. 181, 6441-6448
32. Mo, C., Milla, P., Athenstaedt, K., Ott, R., Balliano, G., Daum, G. & Bard, M. (2003) In yeast sterol biosynthesis the 3-keto reductase protein (Erg27p) is required for oxiclosqualene cyclase (Erg7p) activity. Biochim. Biophys. Acta 1633, 68-74
33. Prein, B., Natter, K. & Kohlwein, S. D. (2000) A novel strategy for constructing N-terminal chromosomal fusions to green fluorescent protein in the yeast Saccharomyces cerevisiae. FEBS Lett. 485, 29-34
34. Leber, R., Zinser, E., Zellnig, G., Paltauf, F. & Daum, G. (1994) Characterization of lipid particles of the yeast, Saccharomyces cerevisiae. Yeast 10, 1421-1428
35. Han, G., Gable, K., Kohlwein, S. D., Beaudoin, F., Napier, J. A. & Dunn, T. M. (2002) The Saccharomyces cerevisiae YBR159w gene encodes the 3-ketoreductase of the microsomal fatty acid elongase. J. Biol. Chem. 277, 35440-35449
36. Kohlwein, S. D., Eder, S., Oh, C. S., Martin, C. E., Gable, K., Bacikova, D. & Dunn, T. (2001) Tsc13p is required for fatty acid elongation and localizes to a novel structure at the nuclear-vacuolar interface in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 109-125
37. Pan, X., Roberts, P., Chen, Y., Kvam, E., Shulga, N., Huang, K., Lemmon, S. & Goldfarb, D. S. (2000) Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1.p Mol. Biol. Cell 11, 2445-2457
38. Wright, R., Basson, M., D'Ari, L. & Rine, J. (1988) Increased amounts of HMG-CoA reductase induce "karmellae": a proliferation of stacked membrane pairs surrounding the yeast nucleus. J. Cell Biol. 107, 101-114
39. Gable, K., Slife, H., Bacikova, D., Monaghan, E. & Dunn, T. M. (2000) Tsc3p is an 80-amino acid protein associated with serine palmitoyltransferase and required for optimal enzyme activity. J. Biol. Chem. 275, 7597-7603
40. Cliften, P., Wang, Y., Mochizuki, D., Miyakawa, T., Wangspa, R., Hughes, J. & Takemoto, J. Y. (1996). SYR2, a gene necessary for syringomycin growth inhibition of Saccharomyces cerevisiae. Microbiology 142, 477-484
41. Guillas, I., Kirchman, P. A., Chuard, R., Pfefferli, M., Jiang, J. C, Jazwinski, S. M. & Conzelmann, A. (2001) C26-CoA-dependent ceramide synthesis of Saccharomyces cerevisiae is operated by Lag1p and Lac1p. EMBO J. 20, 2655-2665
42. Barz, W. P. & Walter, P. (1999) Two endoplasmic reticulum (ER) membrane proteins that facilitate ER-to-Golgi transport of glycosylphosphatidylinositol-anchored proteins. Mol. Biol. Cell 10, 1043-1059
43. Eisenkolb, M., Zenzmaier, C., Leitner, E. & Schneiter, R. (2002) A specific structural requirement for ergosterol in long-chain fatty acid synthesis mutants important for maintaining raft domains in yeast. Mol. Biol. Cell 13, 4414-4428
44. Simons, K. & Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572
45. Thukral, S. K., Eisen, A. & Young, E. T. (1991) Two monomers of yeast transcription factor ADR1 bind a palindromic sequence symmetrically to activate ADH2 expression. Mol. Cell. Biol. 11, 1566-1577
46. Murphy, D. J. & Vance, J. (1999) Mechanisms of lipid-body formation. Trends Biochem. Sci. 24, 109-115
47. Sorger, D., Athenstaedt, K., Hrastnik, C. & Daum, G. (2004). A yeast strain lacking lipid particles bears a defect in ergosterol formation. J. Biol. Chem. 279, 31190-31196
48. Roberts, P., Moshitch-Moshkovitz, S., Kvam, E., O'Toole, E., Winey, M. & Goldfarb, D. S. (2003) Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 129-141
49. Mo, C., Valachovic, M., Randall, S. K., Nickels, J. T. & Bard, M. (2002) Protein-protein interactions among C-4 demethylation enzymes involved in yeast sterol biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 99, 9739-9744
50. Brown, M. S. & Goldstein, J. L. (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331-340
51. Chellappa, R., Kandasamy, P., Oh, C. S., Jiang, Y., Vemula, M. & Martin, C. E. (2001) The membrane proteins, Spt23p and Mga2p, play distinct roles in the activation of Saccharomyces cerevisiae OLE1 gene expression. Fatty acid-mediated regulation of Mga2p activity is independent of its proteolytic processing into a soluble transcription activator. J. Biol. Chem. 276, 43548-43556
52. Hoppe, T., Matuschewski, K., Rape, M., Schlenker, S., Ulrich, H. D. & Jentsch, S. (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102, 577-586
53. Rape, M., Hoppe, T., Gorr, I., Kalocay, M., Richly, H. & Jentsch, S. (2001) Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 107, 667-677
54. Stewart, L. C. & Yaffe, M. P. (1991) A role for unsaturated fatty acids in mitochondrial movement and inheritance. J. Cell Biol. 115, 1249-1257
55. Tatzer, V., Zellnig, G., Kohlwein, S. D. & Schneiter, R. (2002) Lipid-dependent subcellular relocalization of the acyl chain desaturase in yeast. Mol. Biol. Cell 13, 4429-4442