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PMID: 12475962 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A specific structural requirement for ergosterol in long-chain fatty acid synthesis mutants important for maintaining raft domains in yeast.

Molecular biology of the cell ·Vol. 13 ·No. 12 ·2002-12-00 ·Pages 4414-28

Eisenkolb M, Zenzmaier C, Leitner E, Schneiter R

Abstract

Fungal sphingolipids contain ceramide with a very-long-chain fatty acid (C26). To investigate the physiological significance of the C26-substitution on this lipid, we performed a screen for mutants that are synthetically lethal with ELO3. Elo3p is a component of the ER-associated fatty acid elongase and is required for the final elongation cycle to produce C26 from C22/C24 fatty acids. elo3delta mutant cells thus contain C22/C24- instead of the natural C26-substituted ceramide. We now report that under these conditions, an otherwise nonessential, but also fungal-specific, structural modification of the major sterol of yeast, ergosterol, becomes essential, because mutations in ELO3 are synthetically lethal with mutations in ERG6. Erg6p catalyzes the methylation of carbon atom 24 in the aliphatic side chain of sterol. The lethality of an elo3delta erg6delta double mutant is rescued by supplementation with ergosterol but not with cholesterol, indicating a vital structural requirement for the ergosterol-specific methyl group. To characterize this structural requirement in more detail, we generated a strain that is temperature sensitive for the function of Erg6p in an elo3delta mutant background. Examination of raft association of the GPI-anchored Gas1p and plasma membrane ATPase, Pma1p, in the conditional elo3delta erg6(ts) double mutant, revealed a specific defect of the mutant to maintain raft association of preexisting Pma1p. Interestingly, in an elo3delta mutant at 37 degrees C, newly synthesized Pma1p failed to enter raft domains early in the biosynthetic pathway, and upon arrival at the plasma membrane was rerouted to the vacuole for degradation. These observations indicate that the C26 fatty acid substitution on lipids is important for establishing raft association of Pma1p and stabilizing the protein at the cell surface. Analysis of raft lipids in the conditional mutant strain revealed a selective enrichment of ergosterol in detergent-resistant membrane domains, indicating that specific structural determinants on both sterols and sphingolipids are required for their association into raft domains.

MeSH Terms
Acetyltransferases Alleles Cell Membrane/metabolism Cell Survival Cholesterol/metabolism Detergents/pharmacology Ergosterol/chemistry,metabolism Fatty Acids/genetics Genetic Techniques Lipid Metabolism Membrane Microdomains/metabolism Methyltransferases/genetics,metabolism Models, Biological Models, Chemical Mutation Plasmids/metabolism Protein Binding Saccharomyces cerevisiae Proteins/metabolism Sphingolipids/metabolism Temperature Time Factors Yeasts/metabolism
Chemicals
Detergents Fatty Acids Saccharomyces cerevisiae Proteins Sphingolipids Cholesterol Methyltransferases delta 24-sterol methyltransferase Acetyltransferases SUR4 protein, S cerevisiae Ergosterol
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Eisenkolb Marlis
Institute of Biochemistry, Graz University of Technology, A-8010 Graz, Austria.
Zenzmaier Christoph
Leitner Erich
Schneiter Roger
References (59)
59 references, click to expand
  1. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  2. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae.
    Genes Dev. 1994 May 1;8(9):1087-105 PMID: 7926789
  3. The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol.
    Mol Cell Biol. 1989 Aug;9(8):3447-56 PMID: 2677674
  4. Cloning by function: an alternative approach for identifying yeast homologs of genes from other organisms.
    Proc Natl Acad Sci U S A. 1990 Sep;87(17):6629-33 PMID: 2204059
  5. Interaction of cholesterol with various glycerophospholipids and sphingomyelin.
    Biochemistry. 1990 Nov 27;29(47):10670-5 PMID: 2176878
  6. Purification, biosynthesis and cellular localization of a major 125-kDa glycophosphatidylinositol-anchored membrane glycoprotein of Saccharomyces cerevisiae.
    Eur J Biochem. 1991 Jan 30;195(2):439-48 PMID: 1847682
  7. Characterization, quantification and subcellular localization of inositol-containing sphingolipids of the yeast, Saccharomyces cerevisiae.
    Eur J Biochem. 1994 Oct 15;225(2):641-9 PMID: 7957179
  8. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12130-4 PMID: 7991596
  9. Specific sterols required for the internalization step of endocytosis in yeast.
    Mol Biol Cell. 1999 Nov;10(11):3943-57 PMID: 10564282
  10. Brave little yeast, please guide us to thebes: sphingolipid function in S. cerevisiae.
    Bioessays. 1999 Dec;21(12):1004-10 PMID: 10580985
  11. Intracellular transport of GPI-anchored proteins.
    EMBO J. 2000 Jan 4;19(1):10-5 PMID: 10619839
  12. Ceramide in the eukaryotic stress response.
    Trends Cell Biol. 2000 Feb;10(2):73-80 PMID: 10652518
  13. Use of sterol mutants as probes for sterol functions in the yeast, Saccharomyces cerevisiae.
    Crit Rev Biochem Mol Biol. 1999;34(6):399-404 PMID: 10711784
  14. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3254-9 PMID: 10716729
  15. Structure and function of sphingolipid- and cholesterol-rich membrane rafts.
    J Biol Chem. 2000 Jun 9;275(23):17221-4 PMID: 10770957
  16. Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae.
    Mol Biol Cell. 2000 Jul;11(7):2267-81 PMID: 10888667
  17. A mutant plasma membrane ATPase, Pma1-10, is defective in stability at the yeast cell surface.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9104-9 PMID: 11481477
  18. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide.
    J Biol Chem. 2001 Sep 7;276(36):33540-6 PMID: 11432870
  19. Cholesterol interactions with phospholipids in membranes.
    Prog Lipid Res. 2002 Jan;41(1):66-97 PMID: 11694269
  20. Vesicular and nonvesicular transport of ceramide from ER to the Golgi apparatus in yeast.
    J Cell Biol. 2001 Dec 10;155(6):949-59 PMID: 11733544
  21. Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast.
    Mol Biol Cell. 2001 Dec;12(12):4129-38 PMID: 11739806
  22. Proteolytic function of GPI-anchored plasma membrane protease Yps1p in the yeast vacuole and Golgi.
    Traffic. 2001 Dec;2(12):896-907 PMID: 11737827
  23. Quality control in the yeast secretory pathway: a misfolded PMA1 H+-ATPase reveals two checkpoints.
    J Biol Chem. 2002 Jun 7;277(23):21027-40 PMID: 11877403
  24. Ceramide biosynthesis is required for the formation of the oligomeric H+-ATPase Pma1p in the yeast endoplasmic reticulum.
    J Biol Chem. 2002 Jun 21;277(25):22395-401 PMID: 11950838
  25. Sterol-dependent regulation of sphingolipid metabolism in Saccharomyces cerevisiae.
    J Biol Chem. 2002 Jul 19;277(29):26177-84 PMID: 12006573
  26. Beta-D-fructofuranoside fructohydrolase from yeast.
    Methods Enzymol. 1975;42:504-11 PMID: 237205
  27. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1858-62 PMID: 377286
  28. Structural and physiological features of sterols necessary to satisfy bulk membrane and sparking requirements in yeast sterol auxotrophs.
    Arch Biochem Biophys. 1983 Sep;225(2):861-71 PMID: 6354097
  29. A protein kinase antigenically related to pp60v-src possibly involved in yeast cell cycle control: positive in vivo regulation by sterol.
    Proc Natl Acad Sci U S A. 1987 Jun;84(12):4012-6 PMID: 2438691
  30. Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts.
    J Biol Chem. 1989 Mar 5;264(7):3786-93 PMID: 2917977
  31. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae.
    Yeast. 1994 Dec;10(13):1793-808 PMID: 7747518
  32. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C.
    Yeast. 1995 Jan;11(1):53-5 PMID: 7762301
  33. Aerobic isolation of an ERG24 null mutant of Saccharomyces cerevisiae.
    J Bacteriol. 1996 May;178(10):2991-3 PMID: 8631695
  34. The immunosuppressant SR 31747 blocks cell proliferation by inhibiting a steroid isomerase in Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Jun;16(6):2719-27 PMID: 8649379
  35. The extraction and analysis of sterols from yeast.
    Methods Mol Biol. 1996;53:123-31 PMID: 8924974
  36. Cholesterol at different bilayer concentrations can promote or antagonize lateral segregation of phospholipids of differing acyl chain length.
    Biochemistry. 1996 Dec 3;35(48):15198-208 PMID: 8952467
  37. Ceramide profiling of complex lipid mixtures by electrospray ionization mass spectrometry.
    Anal Biochem. 1997 Jan 15;244(2):347-56 PMID: 9025952
  38. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  39. Alternative lipid remodelling pathways for glycosylphosphatidylinositol membrane anchors in Saccharomyces cerevisiae.
    EMBO J. 1997 Jun 16;16(12):3494-505 PMID: 9218792
  40. Lipid remodeling leads to the introduction and exchange of defined ceramides on GPI proteins in the ER and Golgi of Saccharomyces cerevisiae.
    EMBO J. 1997 Jun 16;16(12):3506-18 PMID: 9218793
  41. ELO2 and ELO3, homologues of the Saccharomyces cerevisiae ELO1 gene, function in fatty acid elongation and are required for sphingolipid formation.
    J Biol Chem. 1997 Jul 11;272(28):17376-84 PMID: 9211877
  42. Specific requirements for the ER to Golgi transport of GPI-anchored proteins in yeast.
    J Cell Sci. 1997 Nov;110 ( Pt 21):2703-14 PMID: 9427388
  43. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae.
    Yeast. 1998 Jul;14(10):953-61 PMID: 9717241
  44. Sphingolipid functions in Saccharomyces cerevisiae: comparison to mammals.
    Annu Rev Biochem. 1998;67:27-48 PMID: 9759481
  45. The differential miscibility of lipids as the basis for the formation of functional membrane rafts.
    Biochim Biophys Acta. 1998 Nov 10;1376(3):467-79 PMID: 9805010
  46. Involvement of long chain fatty acid elongation in the trafficking of secretory vesicles in yeast.
    J Cell Biol. 1998 Nov 30;143(5):1167-82 PMID: 9832547
  47. Biochemistry and molecular biology of sterol synthesis in Saccharomyces cerevisiae.
    Crit Rev Biochem Mol Biol. 1999;34(1):33-47 PMID: 10090470
  48. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis.
    Science. 1999 Aug 6;285(5429):901-6 PMID: 10436161
  49. 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. 1999 Aug 23;146(4):741-54 PMID: 10459010
  50. The phosphoinositol sphingolipids of Saccharomyces cerevisiae are highly localized in the plasma membrane.
    J Bacteriol. 1991 May;173(10):3101-8 PMID: 1827112
  51. Three proteolytic systems in the yeast saccharomyces cerevisiae.
    J Biol Chem. 1991 May 5;266(13):7963-6 PMID: 2022624
  52. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface.
    Cell. 1992 Feb 7;68(3):533-44 PMID: 1531449
  53. Structure and cohesive properties of sphingomyelin/cholesterol bilayers.
    Biochemistry. 1992 Feb 25;31(7):2012-20 PMID: 1536844
  54. Multifunctional yeast high-copy-number shuttle vectors.
    Gene. 1992 Jan 2;110(1):119-22 PMID: 1544568
  55. end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae.
    J Cell Biol. 1993 Jan;120(1):55-65 PMID: 8380177
  56. Brefeldin A reversibly inhibits secretion in Saccharomyces cerevisiae.
    J Biol Chem. 1993 Mar 15;268(8):5345-8 PMID: 8449896
  57. General resistance to sterol biosynthesis inhibitors in Saccharomyces cerevisiae.
    Lipids. 1993 Oct;28(10):907-12 PMID: 8246690
  58. Transcriptional control of yeast plasma membrane H(+)-ATPase by glucose. Cloning and characterization of a new gene involved in this regulation.
    J Biol Chem. 1994 Jul 8;269(27):18076-82 PMID: 8027068
  59. Interdigitated bilayer membranes.
    Prog Lipid Res. 1988;27(4):325-59 PMID: 3076241
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2002-12-00
Pages
4414-28
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC138643
Subset
IM
Analysis Services
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