Identification and biophysical characterization of a very-long-chain-fatty- acid-substituted phosphatidylinositol in yeast subcellular membranes

Biochemical Journal

Volumn 381, Issue 3, 2004, Pages 941-949

  Schneiter, Roger ^a   Brügger, Britta ^b   Amann, Clare M ^c   Prestwich, Glenn D ^c   Epand, Raquel F ^d   Zellnig, Günther ^e   Wieland, Felix T ^b   Epand, Richard M ^e  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF UTAH   (United States)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY OF GRAZ   (Austria)

Author keywords

1,2 dielaidoyl sn glycero 3 phosphoethanolamine; Fatty acid; Membrane curvature; Nuclear pore complex; Subcellular membrane; Yeast

Indexed keywords

CELL MEMBRANES; ENZYMES; GLYCEROL; LIPIDS; PHASE TRANSITIONS; SYNTHESIS (CHEMICAL); YEAST;

LIPOSOMES; NUCLEAR MEMBRANES; PLASMA MEMBRANES; YEAST MUTANT;

FATTY ACIDS;

1,2 DIELAIDOYL SN GLYCERO 3 PHOSPHOETHANOLAMINE; CERAMIDE; GLYCEROL; GLYCEROPHOSPHOLIPID; GLYCOSYLPHOSPHATIDYLINOSITOL; LIPOSOME; LONG CHAIN FATTY ACID; PHOSPHATIDYLINOSITOL; UNCLASSIFIED DRUG; VERY LONG CHAIN FATTY ACID;

ARTICLE; CELL MEMBRANE; CELL MUTANT; CELL NUCLEUS MEMBRANE; CELLULAR DISTRIBUTION; DIFFERENTIAL SCANNING CALORIMETRY; ELECTRON MICROSCOPY; FATTY ACID ANALYSIS; ISOLATION PROCEDURE; LIPID ANALYSIS; LIPID COMPOSITION; LIPOGENESIS; MASS SPECTROMETRY; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; YEAST;

ACYLTRANSFERASES; CERAMIDES; FATTY ACIDS; GLYCOSYLPHOSPHATIDYLINOSITOLS; INTRACELLULAR MEMBRANES; LIPIDS; MASS SPECTROMETRY; MODELS, MOLECULAR; NUCLEAR ENVELOPE; PHOSPHATIDYLINOSITOLS; SACCHAROMYCES CEREVISIAE; SERINE C-PALMITOYLTRANSFERASE;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 4344564696     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040320     Document Type: Article

References (46)

1. Singer, S. J. and Micolson, G. L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175, 720-731
2. van Meer, G. (1989) Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5, 247-275
3. Baumgart, T., Hess, S. T. and Webb, W. W. (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature (London) 425, 821-824
4. Munro, S. (2003) Lipid rafts: elusive or illusive? Cell 115, 377-388
5. Mouritsen, O. G. and Bloom, M. (1984) Mattress model of lipid-protein interactions in membranes. Biophys. J. 46, 141-153
6. Bogdanov, M., Heacock, P. N. and Dowhan, W. (2002) A polytopic membrane protein displays a reversible topology dependent on membrane lipid composition. EMBO J. 21, 2107-2116
7. Wente, S. R. (2000) Gatekeepers of the nucleus. Science 288, 1374-1377
8. Marelli, M., Lusk, C. P., Chan, H., Aitchison, J. D. and Wozniak, R. W. (2001) A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J. Cell Biol. 153, 709-724
9. Worman, H. J. and Courvalin, J. C. (2000) The inner nuclear membrane. J. Membr. Biol. 177, 1-11
10. Schneller, R., Hitomi, M., Ivessa, A. S., Fasch, E. V., Kohlwein, S. D. and Tartakoff, A. M. (1996) A yeast acetyl coenzyme A carboxylase mutant links very-long-chain fatty acid synthesis to the structure and function of the nuclear membrane-pore complex. Mol. Cell. Biol. 16, 7161-7172
11. Schneiter, R. and Kohlwein, S. D. (1997) Organelle structure, function, and inheritance in yeast: a role for fatty acid synthesis? Cell 88, 431-434
12. Al-Feel, W., DeMar, J. C. and Wakil, S. J. (2003) A Saccharomyces cerevisiae mutant strain defective in acetyl-CoA carboxylase arrests at the G2/M phase of the cell cycle. Proc. Natl. Acad. Sci. U.S.A. 100, 3095-3100
13. Aitchison, J. D., Blobel, G. and Rout, M. P. (1995) Nup120p: a yeast nucleoporin required for NPC distribution and mRNA transport. J. Cell Biol. 131, 1659-1675
14. Goldstein, A. L., Snay, C. A., Heath, C. V. and Cole, C. N. (1996) Pleiotropic nuclear defects associated with a conditional allele of the novel nucleoporin Rat9p/Nup85p. Mol. Biol. Cell 7, 917-934
15. Siniossoglou, S., Wimmer, C., Rieger, M., Doye, V., Tekotte, H., Weise, C., Emig, S., Segref, A. and Hurt, E. C. (1996) A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84, 265-275
16. Hasslacher, M., Ivessa, A. S., Paltauf, F. and Kohlwein, S. D. (1993) Acetyl-CoA carboxylase from yeast is an essential enzyme and is regulated by factors that control phospholipid metabolism. J. Biol. Chem. 268, 10946-10952
17. Kohlwein, S. D., Eder, S., Oh, C. S., Martin, C. E., Gable, K., Bacikova, D. and 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
18. Lester, R. L. and Dickson, R. C. (1993) Sphingolipids with inositol phosphate-containing head groups. Adv. Lipid Res. 26, 253-274
19. Lester, R. L., Wells, G. B., Oxford, G. and Dickson, R. C. (1993) Mutant strains of Saccharomyces cerevisiae lacking sphingolipids synthesize novel inositol glycerolipids that mimic sphingolipid structure. J. Biol. Chem. 268, 845-856
20. Sipos, G., Reggiori, F., Vionnet, C. and Conzelmann, A. (1997) Alternative lipid remodelling pathways for glycosylphosphatidylinositol membrane anchors in Saccharomyces cerevisiae. EMBO J. 16, 3494-3505
21. Zweytick, D., Leitner, E., Kohlwein, S. D., Yu, C., Rothblatt, J. and Daum, G. (2000) Contribution of Are1p and Are2p to steryl ester synthesis in the yeast Saccharomyces cerevisiae. Eur. J. Biochem. 267, 1075-1082
22. Leidich, S. D., Drapp, D. A. and Orlean, P. (1994) A conditionally lethal yeast mutant blocked at the first step in glycosyl phosphatidylinositol anchor synthesis. J. Biol. Chem. 269, 10193-10196
23. Sandager, L., Gustavsson, M. H., Stahl, U., Dahlqvist, A., Wiberg, E., Banas, A., Lenman, M., Ronne, H. and Stymne, S. (2002) Storage lipid synthesis is non-essential in yeast. J. Biol. Chem. 277, 6478-6482
24. Sütterlin, C., Doering, T. L., Schimmöller, F., Schröder, S. and Riezman, H. (1997) Specific requirements for the ER to Golgi transport of GPI-anchored proteins in yeast. J. Cell Sci. 110, 2703-2714
25. Leidich, S. D., Kostova, Z., Latek, R. R., Costello, L. C., Drapp, D. A., Gray, W., Fassler, J. S. and Orlen, P. (1995) Temperature-sensitive yeast GPI anchoring mutants gpi2 and gpi3 are defective in the synthesis of N-acetylglucosaminyl phosphatidylinositol. J. Biol. Chem. 270, 13029-13035
26. Hurt, E. C., McDowall, A. and Schimmang, T. (1988) Nucleolar and nuclear envelope proteins of the yeast Saccharomyces cerevisiae. Eur. J. Cell Biol. 46, 554-563
27. +-ATPase from plasma membranes of Saccharomyces cerevisiae and Avena sativa roots: purification and reconstitution. Methods Enzymol. 157, 533-544
28. Schneiter, R., Brügger, B., Sandhoff, R., Zellnig, G., Leber, A., Lampl, M., Athenstaedt, K., Hrastnik, C., Eder, S., Daum, G. et al. (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
29. 3). J. Org. Chem. 61, 6305-6312
30. Prestwich, G. D. (1996) Touching the bases: inositol polyphosphate and phosphoinositide affinity probes from glucose. Ace. Chem. Res. 29, 503-513
31. Chen, J., Feng, L. and Prestwich, G. D. (1998) Asymmetric total synthesis of diacyl-and head-group phosphatidylinositol 3-phosphate and 4-phosphate derivatives. J. Org. Chem. 63, 6511-6522
32. Billington, D. C. (1989) Recent developments in the synthesis of myo-inositol phosphates. Chem. Soc. Rev. 18, 83-122
33. Barz, W. P. and 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
34. Gaynor, E. C., Mondesert, G., Grimme, S. J., Reed, S. I., Orlean, P. and Emr, S. D. (1999) MCD4 encodes a conserved endoplasmic reticulum membrane protein essential for glycosylphosphatidylinositol anchor synthesis in yeast. Mol. Biol. Cell 10, 627-648
35. Patton, J. L. and Lester, R. L. (1991) The phosphoinositol sphingolipids of Saccharomyces cerevisiae are highly localized in the plasma membrane. J. Bacteriol. 173, 3101-3108
36. Murata, N., Sato, N. and Takahashi, N. (1984) Very-long-chain fatty acids in phosphatidylserine from higher plant tissue. Biochim. Biophys. Acta 795, 147-150
37. Poulos, A. (1995) Very long chain fatty acids in higher animals - a review. Lipids 30, 1-14
38. Zheng, Z. and Zou, J. (2001) The initial step of the glycerolipid pathway: identification of glycerol 3-phosphate/dihydroxyacetone phosphate dual substrate acyltransferases in Saccharomyces cerevisiae. J. Biol. Chem. 276, 41710-41716
39. Brugger, B., Erben, G., Sandhoff, R., Wieland, F. T. and Lehmann, W. D. (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 94, 2339-2344
40. Epand, R. M. (1985) Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry 24, 7092-7095
41. Epand, R. M., Robinson, K. S., Andrews, M. E. and Epand, R. F. (1989) Dependence of the bilayer to hexagonal phase transition on amphiphile chain length. Biochemistry 28, 9398-9402
42. Epand, R. M. and Bryszewska, M. (1988) Modulation of the bilayer to hexagonal phase transition and solvation of phosphatidylethanolamines in aqueous salt solutions. Biochemistry 27, 8776-8779
43. Fahrenkrog, B., Hurt, E. C., Aebi, U. and Pante, N. (1998) Molecular architecture of the yeast nuclear pore complex: localization of Nsp1p subcomplexes. J. Cell Biol. 143, 577-588
44. Yang, Q., Rout, M. P. and Akey, C. W. (1998) Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell 1, 223-234
45. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M. F., Ravazzola, M., Amherdt, M. and Schekman, R. (1994) COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907
46. Mulholland, J., Preuss, D., Moon, A., Wong, A., Drubin, D. and Botstein, D. (1994) Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 125, 381-391