Saccharomyces cerevisiae is dependent on vesicular traffic between the Golgi apparatus and the vacuole when inositolphosphorylceramide synthase aur1 is inactivated

Eukaryotic Cell

Volumn 14, Issue 12, 2015, Pages 1203-1216

  Voynova, Natalia S ^a,c   Roubaty, Carole ^a   Vazquez, Hector M ^a   Mallela, Shamroop K ^a   Ejsing, Christer S ^b   Conzelmann, Andreas ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

AUREOBASIDIN A; CERAMIDE; DEPSIPEPTIDE; DOXYCYCLINE; FAT DROPLET; GLYCOSPHINGOLIPID; GLYCOSYLTRANSFERASE; INOSITOLPHOSPHORYLCERAMIDE; MEPACRINE; PHOSPHATIDYLINOSITOL-CERAMIDE PHOSPHOINOSITOL TRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN; SPHINGOLIPID;

ALLELE; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL VACUOLE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; EPISTASIS; GENE DELETION; GENE ONTOLOGY; GENETIC SCREENING; GENETICS; GOLGI COMPLEX; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SCREENING; HYDROLYSIS; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE;

ALLELES; BIOLOGICAL TRANSPORT; BIOSYNTHETIC PATHWAYS; CERAMIDES; DEPSIPEPTIDES; DOXYCYCLINE; EPISTASIS, GENETIC; GENE DELETION; GENE ONTOLOGY; GENETIC TESTING; GLYCOSPHINGOLIPIDS; GOLGI APPARATUS; HEXOSYLTRANSFERASES; HIGH-THROUGHPUT SCREENING ASSAYS; HYDROLYSIS; LIPID DROPLETS; MUTATION; QUINACRINE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPHINGOLIPIDS; TRANSPORT VESICLES; VACUOLES;

EID: 84948974733     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00117-15     Document Type: Article

References (67)

1. Buede R, Rinker-Schaffer C, Pinto WJ, Lester RL, Dickson RC. 1991. Cloning and characterization of LCB1, a Saccharomyces gene required for biosynthesis of the long-chain base component of sphingolipids. J Bacteriol 173:4325-4332.
2. 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.
3. Beeler TJ, Fu D, Rivera J, Monaghan E, Gable K, Dunn TM. 1997. SUR1 (CSG1/BCL21), a gene necessary for growth of Saccharomyces cerevisiae in the presence of high Ca2+ concentrations at 37 degrees C, is required for mannosylation of inositolphosphorylceramide. Mol Gen Genet 255:570-579. http://dx.doi.org/10.1007/s004380050530.
4. Uemura S, Kihara A, Inokuchi J, Igarashi Y. 2003. Csg1p and newly identified Csh1p function in mannosylinositol phosphorylceramide synthesis by interacting with Csg2p. J Biol Chem 278:45049-45055. http://dx.doi.org/10.1074/jbc.M305498200.
5. Lisman Q, Pomorski T, Vogelzangs C, Urli-Stam D, de Cocq van Delwijnen W, Holthuis JC. 2004. Protein sorting in the late Golgi of Saccharomyces cerevisiae does not require mannosylated sphingolipids. J Biol Chem 279:1020-1029. http://dx.doi.org/10.1074/jbc.M306119200.
6. Heidler SA, Radding JA. 1995. The AUR1 gene in Saccharomyces cerevisiae encodes dominant resistance to the antifungal agent aureobasidin A (LY295337). Antimicrob Agents Chemother 39:2765-2769. http://dx.doi.org/10.1128/AAC.39.12.2765.
7. Hashida-Okado T, Ogawa A, Endo M, Yasumoto R, Takesako K, Kato I. 1996. AUR1, a novel gene conferring aureobasidin resistance on Saccharomyces cerevisiae: a study of defective morphologies in Aur1pdepleted cells. Mol Gen Genet 251:236-244.
8. 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.
9. 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 cerevisae. Mol Biol Cell 12:3417-3427. http://dx.doi.org/10.1091/mbc.12.11.3417.
10. Nagiec MM, Wells GB, Lester RL, Dickson RC. 1993. A suppressor gene that enables Saccharomyces cerevisiae to grow without making sphingolipids encodes a protein that resembles an Escherichia coli fatty acyltransferase. J Biol Chem 268:22156-22163.
11. Lester RL, Wells GB, Oxford G, Dickson RC. 1993. Mutant strains of Saccharomyces cerevisiae lacking sphingolipids synthesize novel inositol glycerophospholipids that mimic sphingolipid structures. J Biol Chem 268:845-856.
12. Gaigg B, Toulmay A, Schneiter R. 2006. Very long-chain fatty acidcontaining lipids rather than sphingolipids per se are required for raft association and stable surface transport of newly synthesized plasma membrane ATPase in yeast. J Biol Chem 281:34135-34145. http://dx.doi.org/10.1074/jbc.M603791200.
13. Vionnet C, Roubaty C, Ejsing CS, Knudsen J, Conzelmann A. 2011. Yeast cells lacking all known ceramide synthases continue to make complex sphingolipids and to incorporate ceramides into glycosylphosphatidylinositol (GPI) anchors. J Biol Chem 286:6769-6779. http://dx.doi.org/10.1074/jbc.M110.176875.
14. Kajiwara K, Muneoka T, Watanabe Y, Karashima T, Kitagaki H, Funato K. 2012. Perturbation of sphingolipid metabolism induces endoplasmic reticulum stress-mediated mitochondrial apoptosis in budding yeast. Mol Microbiol 86:1246-1261. http://dx.doi.org/10.1111/mmi.12056.
15. Takesako K, Kuroda H, Inoue T, Haruna F, Yoshikawa Y, Kato I, Uchida K, Hiratani T, Yamaguchi H. 1993. Biological properties of aureobasidin A, a cyclic depsipeptide antifungal antibiotic. J Antibiot (Tokyo) 46:1414-1420. http://dx.doi.org/10.7164/antibiotics.46.1414.
16. Mao C, Xu R, Bielawska A, Szulc ZM, Obeid LM. 2000. Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide. J Biol Chem 275:31369-31378. http://dx.doi.org/10.1074/jbc.M003683200.
17. 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. http://dx.doi.org/10.1074/jbc.M112.444802.
18. Roelants FM, Baltz AG, Trott AE, Fereres S, Thorner J. 2010. A protein kinase network regulates the function of aminophospholipid flippases. Proc Natl Acad Sci U S A 107:34-39. http://dx.doi.org/10.1073/pnas.0912497106.
19. Belli G, Gari E, Aldea M, Herrero E. 1998. Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline- regulatable dual expression system. Yeast 14:1127-1138.
20. Voth WP, Jiang YW, Stillman DJ. 2003. New ‘marker swap’ plasmids for converting selectable markers on budding yeast gene disruptions and plasmids. Yeast 20:985-993. http://dx.doi.org/10.1002/yea.1018.
21. Dittmar JC, Reid RJ, Rothstein R. 2010. ScreenMill: a freely available software suite for growth measurement, analysis and visualization of highthroughput screen data. BMC Bioinformatics 11:353. http://dx.doi.org/10.1186/1471-2105-11-353.
22. 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. http://dx.doi.org/10.1002/jms.997.
23. 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. Proc Natl Acad Sci U S A 106:2136-2141. http://dx.doi.org/10.1073/pnas.0811700106.
24. Voynova NS, Mallela SK, Vazquez HM, Cerantola V, Sonderegger M, Knudsen J, Ejsing CS, Conzelmann A. 2014. Characterization of yeast mutants lacking alkaline ceramidases YPC1 and YDC1. FEMS Yeast Res 14:776-788. http://dx.doi.org/10.1111/1567-1364.12169.
25. Vazquez HM, Vionnet C, Roubaty C, Conzelmann A. 2014. Cdc1 removes the ethanolaminephosphate of the first mannose of GPI anchors and thereby facilitates the integration of GPI proteins into the yeast cell wall. Mol Biol Cell 25:3375-3388. http://dx.doi.org/10.1091/mbc.E14-06-1033.
26. Haak D, Gable K, Beeler T, Dunn T. 1997. Hydroxylation of Saccharomyces cerevisiae ceramides requires Sur2p and Scs7p. J Biol Chem 272: 29704-29710. http://dx.doi.org/10.1074/jbc.272.47.29704.
27. Rajakumari S, Rajasekharan R, Daum G. 2010. Triacylglycerol lipolysis is linked to sphingolipid and phospholipid metabolism of the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1801:1314-1322. http://dx.doi.org/10.1016/j.bbalip.2010.08.004.
28. 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. http://dx.doi.org/10.1111/j.1365-2958.2009.06628.x.
29. Jesch SA, Gaspar ML, Stefan CJ, Aregullin MA, Henry SA. 2010. Interruption of inositol sphingolipid synthesis triggers Stt4p-dependent protein kinase C signaling. J Biol Chem 285:41947-41960. http://dx.doi.org/10.1074/jbc.M110.188607.
30. Berchtold D, Piccolis M, Chiaruttini N, Riezman I, Riezman H, Roux A, Walther TC, Loewith R. 2012. Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis. Nat Cell Biol 14:542-547. http://dx.doi.org/10.1038/ncb2480.
31. de Nobel H, Ruiz C, Martin H, Morris W, Brul S, Molina M, Klis FM. 2000. Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2-lacZ expression, glucanase resistance and thermotolerance. Microbiology 146: 2121-2132. http://dx.doi.org/10.1099/00221287-146-9-2121.
32. Epstein S, Kirkpatrick CL, Castillon GA, Muniz M, Riezman I, David FP, Wollheim CB, Riezman H. 2012. Activation of the unfolded protein response pathway causes ceramide accumulation in yeast and INS-1E insulinoma cells. J Lipid Res 53:412-420. http://dx.doi.org/10.1194/jlr.M022186.
33. Mandala SM, Thornton RA, Frommer BR, Curotto JE, Rozdilsky W, Kurtz MB, Giacobbe RA, Bills GF, Cabello MA, Martin I, et al. 1995. The discovery of australifungin, a novel inhibitor of sphinganine Nacyltransferase from Sporormiella australis. Producing organism, fermentation, isolation, and biological activity. J Antibiot (Tokyo) 48:349-356.
34. 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.
35. Niles BJ, Joslin AC, Fresques T, Powers T. 2014. TOR complex 2-Ypk1 signaling maintains sphingolipid homeostasis by sensing and regulating ROS accumulation. Cell Rep 6:541-552. http://dx.doi.org/10.1016/j.celrep.2013.12.040.
36. Milgrom E, Diab H, Middleton F, Kane PM. 2007. Loss of vacuolar proton-translocating ATPase activity in yeast results in chronic oxidative stress. J Biol Chem 282:7125-7136.
37. Vallee B, Riezman H. 2005. Lip1p: a novel subunit of acyl-CoA ceramide synthase. EMBO J 24:730-741. http://dx.doi.org/10.1038/sj.emboj.7600562.
38. Tani M, Kuge O. 2010. Requirement of a specific group of sphingolipidmetabolizing enzyme for growth of yeast Saccharomyces cerevisiae under impaired metabolism of glycerophospholipids. Mol Microbiol 78:395-413. http://dx.doi.org/10.1111/j.1365-2958.2010.07340.x.
39. 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. http://dx.doi.org/10.1093/jb/mvq090.
40. 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. http://dx.doi.org/10.1016/j.bbrc.2011.11.138.
41. Kajiwara K, Watanabe R, Pichler H, Ihara K, Murakami S, Riezman H, Funato K. 2008. Yeast ARV1 is required for efficient delivery of an early GPI intermediate to the first mannosyltransferase during GPI assembly and controls lipid flow from the endoplasmic reticulum. Mol Biol Cell 19:2069-2082. http://dx.doi.org/10.1091/mbc.E07-08-0740.
42. Swinnen E, Wilms T, Idkowiak-Baldys J, Smets B, De Snijder P, Accardo S, Ghillebert R, Thevissen K, Cammue B, De Vos D, Bielawski J, Hannun YA, Winderickx J. 2014. The protein kinase Sch9 is a key regulator of sphingolipid metabolism in Saccharomyces cerevisiae. Mol Biol Cell 25:196-211. http://dx.doi.org/10.1091/mbc.E13-06-0340.
43. Khakhina S, Johnson SS, Manoharlal R, Russo SB, Blugeon C, Lemoine S, Sunshine AB, Dunham MJ, Cowart LA, Devaux F, Moye-Rowley WS. 2015. Control of plasma membrane permeability by ABC transporters. Eukaryot Cell 14:442-453. http://dx.doi.org/10.1128/EC.00021-15.
44. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, Andrews B, Tyers M, Boone C. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368. http://dx.doi.org/10.1126/science.1065810.
45. Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, Young J, Berriz GF, Brost RL, Chang M, Chen Y, Cheng X, Chua G, Friesen H, Goldberg DS, Haynes J, Humphries C, He G, Hussein S, Ke L, Krogan N, Li Z, Levinson JN, Lu H, Menard P, Munyana C, Parsons AB, Ryan O, Tonikian R, Roberts T, Sdicu AM, Shapiro J, Sheikh B, Suter B, Wong SL, Zhang LV, Zhu H, Burd CG, Munro S, Sander C, Rine J, Greenblatt J, Peter M, Bretscher A, Bell G, Roth FP, Brown GW, Andrews B, Bussey H, Boone C. 2004. Global mapping of the yeast genetic interaction network. Science 303:808-813. http://dx.doi.org/10.1126/science.1091317.
46. Kane PM. 2006. The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol Mol Biol Rev 70:177-191. http://dx.doi.org/10.1128/MMBR.70.1.177-191.2006.
47. Munn AL, Riezman H. 1994. Endocytosis is required for the growth of vacuolar H(+)-ATPase-defective yeast: identification of six new END genes. J Cell Biol 127:373-386. http://dx.doi.org/10.1083/jcb.127.2.373.
48. Young BP, Shin JJ, Orij R, Chao JT, Li SC, Guan XL, Khong A, Jan E, Wenk MR, Prinz WA, Smits GJ, Loewen CJ. 2010. Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 329:1085-1088. http://dx.doi.org/10.1126/science.1191026.
49. Smardon AM, Kane PM. 2014. Loss of vacuolar H+-ATPase activity in organelles signals ubiquitination and endocytosis of the yeast plasma membrane proton pump Pma1p. J Biol Chem 289:32316-32326. http://dx.doi.org/10.1074/jbc.M114.574442.
50. Villa-Garcia MJ, Choi MS, Hinz FI, Gaspar ML, Jesch SA, Henry SA. 2011. Genome-wide screen for inositol auxotrophy in Saccharomyces cerevisiae implicates lipid metabolism in stress response signaling. Mol Genet Genomics 285:125-149. http://dx.doi.org/10.1007/s00438-010-0592-x.
51. Rothman JH, Yamashiro CT, Raymond CK, Kane PM, Stevens TH. 1989. Acidification of the lysosome-like vacuole and the vacuolar H+- ATPase are deficient in two yeast mutants that fail to sort vacuolar proteins. J Cell Biol 109:93-100. http://dx.doi.org/10.1083/jcb.109.1.93.
52. Weisman LS, Bacallao R, Wickner W. 1987. Multiple methods of visualizing the yeast vacuole permit evaluation of its morphology and inheritance during the cell cycle. J Cell Biol 105:1539-1547. http://dx.doi.org/10.1083/jcb.105.4.1539.
53. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M, Deshpande R, Li Z, Lin ZY, Liang W, Marback M, Paw J, San Luis BJ, Shuteriqi E, Tong AH, van Dyk N, Wallace IM, Whitney JA, Weirauch MT, Zhong G, Zhu H, Houry WA, Brudno M, Ragibizadeh S, Papp B, Pal C, Roth FP, Giaever G, Nislow C, Troyanskaya OG, Bussey H, Bader GD, Gingras AC, Morris QD, Kim PM, Kaiser CA, Myers CL, Andrews BJ, Boone C. 2010. The genetic landscape of a cell. Science 327:425-431. http://dx.doi.org/10.1126/science.1180823.
54. Hoppins S, Collins SR, Cassidy-Stone A, Hummel E, Devay RM, Lackner LL, Westermann B, Schuldiner M, Weissman JS, Nunnari J. 2011. A mitochondrial-focused genetic interaction map reveals a scaffoldlike complex required for inner membrane organization in mitochondria. J Cell Biol 195:323-340. http://dx.doi.org/10.1083/jcb.201107053.
55. Hillenmeyer ME, Fung E, Wildenhain J, Pierce SE, Hoon S, Lee W, Proctor M, St Onge RP, Tyers M, Koller D, Altman RB, Davis RW, Nislow C, Giaever G. 2008. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320:362-365. http://dx.doi.org/10.1126/science.1150021.
56. Han G, Gable K, Yan L, Allen MJ, Wilson WH, Moitra P, Harmon JM, Dunn TM. 2006. Expression of a novel marine viral single-chain serine palmitoyltransferase and construction of yeast and mammalian singlechain chimera. J Biol Chem 281:39935-39942. http://dx.doi.org/10.1074/jbc.M609365200.
57. Adeyo O, Horn PJ, Lee S, Binns DD, Chandrahas A, Chapman KD, Goodman JM. 2011. The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J Cell Biol 192:1043-1055. http://dx.doi.org/10.1083/jcb.201010111.
58. Dickson RC, Sumanasekera C, Lester RL. 2006. Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45:447-465. http://dx.doi.org/10.1016/j.plipres.2006.03.004.
59. Cunningham KW, Fink GR. 1994. Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2_ ATPases. J Cell Biol 124:351-363. http://dx.doi.org/10.1083/jcb.124.3.351.
60. Obara K, Kojima R, Kihara A. 2013. Effects on vesicular transport pathways at the late endosome in cells with limited very long-chain fatty acids. J Lipid Res 54:831-842. http://dx.doi.org/10.1194/jlr.M034678.
61. Tabuchi M, Audhya A, Parsons AB, Boone C, Emr SD. 2006. The phosphatidylinositol 4,5-biphosphate and TORC2 binding proteins Slm1 and Slm2 function in sphingolipid regulation. Mol Cell Biol 26:5861-5875. http://dx.doi.org/10.1128/MCB.02403-05.
62. Roelants FM, Breslow DK, Muir A, Weissman JS, Thorner J. 2011. Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 108:19222-19227. http://dx.doi.org/10.1073/pnas.1116948108.
63. Muir A, Ramachandran S, Roelants FM, Timmons G, Thorner J. 2014. TORC2-dependent protein kinase Ypk1 phosphorylates ceramide synthase to stimulate synthesis of complex sphingolipids. ELife 3. http://dx.doi.org/10.7554/eLife.03779.
64. Breslow DK, Collins SR, Bodenmiller B, Aebersold R, Simons K, Shevchenko A, Ejsing CS, Weissman JS. 2010. Orm family proteins mediate sphingolipid homeostasis. Nature 463:1048-1053. http://dx.doi.org/10.1038/nature08787.
65. Gururaj C, Federman R, Chang A. 2013. Orm proteins integrate multiple signals to maintain sphingolipid homeostasis. J Biol Chem 288:20453-20463. http://dx.doi.org/10.1074/jbc.M113.472860.
66. Tanida I, Hasegawa A, Iida H, Ohya Y, Anraku Y. 1995. Cooperation of calcineurin and vacuolar H(+)-ATPase in intracellular Ca2_ homeostasis of yeast cells. J Biol Chem 270:10113-10119. http://dx.doi.org/10.1074/jbc.270.17.10113.
67. Dickson RC. 2010. Roles for sphingolipids in Saccharomyces cerevisiae. Adv Exp Med Biol 688:217-231. http://dx.doi.org/10.1007/978-1-4419-6741-1_15.