Characterization of yeast mutants lacking alkaline ceramidases YPC1 and YDC1

FEMS Yeast Research

Volumn 14, Issue 5, 2014, Pages 776-788

  Voynova, Natalia S ^a,c   Mallela, Shamroop K ^a   Vazquez, Hector M ^a   Cerantola, Vanessa ^a,d   Sonderegger, Mélanie ^a   Knudsen, Jens ^b   Ejsing, Christer S ^b   Conzelmann, Andreas ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d Philip Morris Products SA   (Switzerland)

Author keywords

Aureobasidin A; Chronological life span; Secretion; Sphingolipid; Synthetic genetic array; Vesicular traffic

Indexed keywords

ALKALINE CERAMIDASE; ALKALINE DIHYDROCERAMIDASE, S CEREVISIAE; AMIDASE; CERAMIDE; SACCHAROMYCES CEREVISIAE PROTEIN; YPC1 PROTEIN, S CEREVISIAE;

ENZYMOLOGY; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SACCHAROMYCES CEREVISIAE;

ALKALINE CERAMIDASE; AMIDOHYDROLASES; CERAMIDES; GENE KNOCKOUT TECHNIQUES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84905585389     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/1567-1364.12169     Document Type: Article

References (59)

1. Aerts AM, Francois IE, Bammens L, Cammue BP, Smets B, Winderickx J, Accardo S, De Vos DE & Thevissen K (2006) Level of M(IP)2C sphingolipid affects plant defensin sensitivity, oxidative stress resistance and chronological life-span in yeast. FEBS Lett 580: 1903-1907.
2. Almeida T, Marques M, Mojzita D et al. (2008) Isc1p plays a key role in hydrogen peroxide resistance and chronological lifespan through modulation of iron levels and apoptosis. Mol Biol Cell 19: 865-876.
3. Bagnat M, Keranen S, Shevchenko A, Shevchenko A & Simons K (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. P Natl Acad Sci USA 97: 3254-3259.
4. Bonangelino CJ, Chavez EM & Bonifacino JS (2002) Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol Biol Cell 13: 2486-2501.
5. Cerantola V, Guillas I, Roubaty C, Vionnet C, Uldry D, Knudsen J & Conzelmann A (2009) Aureobasidin A arrests growth of yeast cells through both ceramide intoxication and deprivation of essential inositolphosphorylceramides. Mol Microbiol 71: 1523-1537.
6. Chung N, Jenkins G, Hannun YA, Heitman J & Obeid LM (2000) Sphingolipids signal heat stress-induced ubiquitin-dependent proteolysis. J Biol Chem 275: 17229-17232.
7. Chung N, Mao C, Heitman J, Hannun YA & Obeid LM (2001) Phytosphingosine as a specific inhibitor of growth and nutrient import in Saccharomyces cerevisiae. J Biol Chem 276: 35614-35621.
8. Collins SR, Roguev A & Krogan NJ (2010) Quantitative genetic interaction mapping using the E-MAP approach. Methods Enzymol 470: 205-231.
9. Costa VM, Amorim MA, Quintanilha A & Moradas-Ferreira P (2002) Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. Free Radic Biol Med 33: 1507-1515.
10. DeLuna A, Vetsigian K, Shoresh N, Hegreness M, Colon-Gonzalez M, Chao S & Kishony R (2008) Exposing the fitness contribution of duplicated genes. Nat Genet 40: 676-681.
11. Dickson RC (2010) Roles for sphingolipids in Saccharomyces cerevisiae. Adv Exp Med Biol 688: 217-231.
12. Dickson RC, Sumanasekera C & Lester RL (2006) Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45: 447-465.
13. Dittmar JC, Reid RJ & Rothstein R (2010) ScreenMill: a freely available software suite for growth measurement, analysis and visualization of high-throughput screen data. BMC Bioinformatics 11: 353.
14. Dunn R, Klos DA, Adler AS & Hicke L (2004) The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J Cell Biol 165: 135-144.
15. Ejsing CS, Moehring T, Bahr U, Duchoslav E, Karas M, Simons K & Shevchenko A (2006) Collision-induced dissociation pathways of yeast sphingolipids and their molecular profiling in total lipid extracts: a study by quadrupole TOF and linear ion trap-orbitrap mass spectrometry. J Mass Spectrom 41: 372-389.
16. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, Klemm RW, Simons K & Shevchenko A (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. P Natl Acad Sci USA 106: 2136-2141.
17. Endo M, Takesako K, Kato I & Yamaguchi H (1997) Fungicidal action of aureobasidin A, a cyclic depsipeptide antifungal antibiotic, against Saccharomyces cerevisiae. Antimicrob Agents Chemother 41: 672-676.
18. Fröhlich F, Moreira K, Aguilar PS, Hubner NC, Mann M, Walter P & Walther TC (2009) A genome-wide screen for genes affecting eisosomes reveals Nce102 function in sphingolipid signaling. J Cell Biol 185: 1227-1242.
19. Gaigg B, Timischl B, Corbino L & Schneiter R (2005) Synthesis of sphingolipids with very long chain fatty acids but not ergosterol is required for routing of newly synthesized plasma membrane ATPase to the cell surface of yeast. J Biol Chem 280: 22515-22522.
20. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D & Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
21. Grossmann G, Malinsky J, Stahlschmidt W, Loibl M, Weig-Meckl I, Frommer WB, Opekarova M & Tanner W (2008) Plasma membrane microdomains regulate turnover of transport proteins in yeast. J Cell Biol 183: 1075-1088.
22. Hanson BA & Lester RL (1980) The extraction of inositol-containing phospholipids and phosphatidylcholine from Saccharomyces cerevisiae and Neurospora crassa. J Lipid Res 21: 309-315.
23. Higgins VJ, Alic N, Thorpe GW, Breitenbach M, Larsson V & Dawes IW (2002) Phenotypic analysis of gene deletant strains for sensitivity to oxidative stress. Yeast 19: 203-214.
24. Hillenmeyer ME, Fung E, Wildenhain J et al. (2008) The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320: 362-365.
25. Horvath A, Sutterlin C, Manning-Krieg U, Movva NR & Riezman H (1994) Ceramide synthesis enhances transport of GPI-anchored proteins to the Golgi apparatus in yeast. EMBO J 13: 3687-3695.
26. Huang X, Liu J & Dickson RC (2012) Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet 8: e1002493.
27. Huang X, Liu J, Withers BR, Samide AJ, Leggas M & Dickson RC (2013) Reducing signs of aging and increasing lifespan by drug synergy. Aging Cell 12: 652-660.
28. Kitagaki H, Cowart LA, Matmati N, Vaena de Avalos S, Novgorodov SA, Zeidan YH, Bielawski J, Obeid LM & Hannun YA (2007) Isc1 regulates sphingolipid metabolism in yeast mitochondria. Biochim Biophys Acta 1768: 2849-2861.
29. Kitagaki H, Cowart LA, Matmati N, Montefusco D, Gandy J, de Avalos SV, Novgorodov SA, Zheng J, Obeid LM & Hannun YA (2009) ISC1-dependent metabolic adaptation reveals an indispensable role for mitochondria in induction of nuclear genes during the diauxic shift in Saccharomyces cerevisiae. J Biol Chem 284: 10818-10830.
30. Laschober GT, Ruli D, Hofer E et al. (2010) Identification of evolutionarily conserved genetic regulators of cellular aging. Aging Cell 9: 1084-1097.
31. Lester RL, Withers BR, Schultz MA & Dickson RC (2013) Iron, glucose and intrinsic factors alter sphingolipid composition as yeast cells enter stationary phase. Biochim Biophys Acta 1831: 726-736.
32. Lewis MJ, Nichols BJ, Prescianotto-Baschong C, Riezman H & Pelham HR (2000) Specific retrieval of the exocytic SNARE Snc1p from early yeast endosomes. Mol Biol Cell 11: 23-38.
33. Lin CH, MacGurn JA, Chu T, Stefan CJ & Emr SD (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135: 714-725.
34. Longo VD, Shadel GS, Kaeberlein M & Kennedy B (2012) Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab 16: 18-31.
35. Malinska K, Malinsky J, Opekarova M & Tanner W (2003) Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol Biol Cell 14: 4427-4436.
36. Manford AG, Stefan CJ, Yuan HL, Macgurn JA & Emr SD (2012) ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell 23: 1129-1140.
37. Mao C & Obeid LM (2008) Ceramidases: regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine-1-phosphate. Biochim Biophys Acta 1781: 424-434.
38. Mao C, Xu R, Bielawska A & Obeid LM (2000a) Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity. J Biol Chem 275: 6876-6884.
39. Mao C, Xu R, Bielawska A, Szulc ZM & Obeid LM (2000b) Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide. J Biol Chem 275: 31369-31378.
40. Matmati N, Metelli A, Tripathi K, Yan S, Mohanty BK & Hannun YA (2013) Identification of c18:1-phytoceramide as the candidate lipid mediator for hydroxyurea resistance in yeast. J Biol Chem 288: 17272-17284.
41. Montefusco DJ, Chen L, Matmati N, Lu S, Newcomb B, Cooper GF, Hannun YA & Lu X (2013) Distinct signaling roles of ceramide species in yeast revealed through systematic perturbation and systems biology analyses. Sci Signal 6: rs14.
42. Montefusco DJ, Matmati N & Hannun YA (2014) The yeast sphingolipid signaling landscape. Chem Phys Lipids 177: 26-40.
43. Nagiec MM, Nagiec EE, Baltisberger JA, Wells GB, Lester RL & Dickson RC (1997) Sphingolipid synthesis as a target for antifungal drugs. Complementation of the inositol phosphorylceramide synthase defect in a mutant strain of Saccharomyces cerevisiae by the AUR1 gene. J Biol Chem 272: 9809-9817.
44. Natter K, Leitner P, Faschinger A, Wolinski H, McCraith S, Fields S & Kohlwein SD (2005) The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy. Mol Cell Proteomics 4: 662-672.
45. Powers RWR, Kaeberlein M, Caldwell SD, Kennedy BK & Fields S (2006) Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev 20: 174-184.
46. Proszynski TJ, Klemm RW, Gravert M et al. (2005) A genome-wide visual screen reveals a role for sphingolipids and ergosterol in cell surface delivery in yeast. P Natl Acad Sci USA 102: 17981-17986.
47. Ramachandra N & Conzelmann A (2013) Membrane topology of yeast alkaline ceramidase YPC1. Biochem J 452: 585-594.
48. Sawai H, Okamoto Y, Luberto C, Mao C, Bielawska A, Domae N & Hannun YA (2000) Identification of ISC1 (YER019w) as inositol phosphosphingolipid phospholipase C in Saccharomyces cerevisiae. J Biol Chem 275: 39793-39798.
49. Schorling S, Vallee B, Barz WP, Riezman H & Oesterhelt D (2001) Lag1p and Lac1p are essential for the Acyl-CoA-dependent ceramide synthase reaction in Saccharomyces cerevisiae. Mol Biol Cell 12: 3417-3427.
50. Stefan CJ & Blumer KJ (1999) A syntaxin homolog encoded by VAM3 mediates down-regulation of a yeast G protein-coupled receptor. J Biol Chem 274: 1835-1841.
51. Tani M & Kuge O (2010) Defect of synthesis of very long-chain fatty acids confers resistance to growth inhibition by inositol phosphorylceramide synthase repression in yeast Saccharomyces cerevisiae. J Biochem 148: 565-571.
52. Tani M & Kuge O (2012) Hydroxylation state of fatty acid and long-chain base moieties of sphingolipid determine the sensitivity to growth inhibition due to AUR1 repression in Saccharomyces cerevisiae. Biochem Biophys Res Commun 417: 673-678.
53. Vaena de Avalos S, Okamoto Y & Hannun YA (2004) Activation and localization of inositol phosphosphingolipid phospholipase C, Isc1p, to the mitochondria during growth of Saccharomyces cerevisiae. J Biol Chem 279: 11537-11545.
54. Vaena de Avalos S, Su X, Zhang M, Okamoto Y, Dowhan W & Hannun YA (2005) The phosphatidylglycerol/cardiolipin biosynthetic pathway is required for the activation of inositol phosphosphingolipid phospholipase C, Isc1p, during growth of Saccharomyces cerevisiae. J Biol Chem 280: 7170-7177.
55. Watanabe R, Funato K, Venkataraman K, Futerman AH & Riezman H (2002) Sphingolipids are required for the stable membrane association of glycosylphosphatidylinositol-anchored proteins in yeast. J Biol Chem 277: 49538-49544.
56. Wolfe KH & Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387: 708-713.
57. Yang Q, Gong ZJ, Zhou Y et al. (2010) Role of Drosophila alkaline ceramidase (Dacer) in Drosophila development and longevity. Cell Mol Life Sci 67: 1477-1490.
58. Young BP, Shin JJ, Orij R et al. (2010) Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 329: 1085-1088.
59. Zanolari B, Friant S, Funato K, Sutterlin C, Stevenson BJ & Riezman H (2000) Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J 19: 2824-2833.