Requirement of a specific group of sphingolipid-metabolizing enzyme for growth of yeast Saccharomyces cerevisiae under impaired metabolism of glycerophospholipidsmmi

Molecular Microbiology

Volumn 78, Issue 2, 2010, Pages 395-413

  Tani, Motohiro ^a,b   Kuge, Osamu ^a,c  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUREOBASIDIN A; BACTERIAL PROTEIN; GLYCEROPHOSPHOLIPID; PHOSPHATIDYLSERINE; SAC1 PROTEIN; SPHINGOLIPID; UNCLASSIFIED DRUG;

ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; FUNGUS GROWTH; MUTATIONAL ANALYSIS; NONHUMAN; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

DEPSIPEPTIDES; GENE DELETION; GENETIC COMPLEMENTATION TEST; GLYCEROPHOSPHOLIPIDS; PHOSPHORIC MONOESTER HYDROLASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPHINGOLIPIDS;

SACCHAROMYCES CEREVISIAE;

EID: 78649365490     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07340.x     Document Type: Article

References (69)

1. 2+ concentrations at 37 degrees C, is required for mannosylation of inositolphosphorylceramide. Mol Gen Genet 255: 570-579.
2. Belli, G., Gari, E., Aldea, M., and Herrero, E. (1998) Functional analysis of yeast essential genes using a promotersubstitution cassette and the tetracycline-regulatable dual expression system. Yeast 14: 1127-1138.
3. Birner, R., Burgermeister, M., Schneiter, R., and Daum, G. (2001) Roles of phosphatidylethanolamine and of its several biosynthetic pathways in Saccharomyces cerevisiae. Mol Biol Cell 12: 997-1007.
4. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., and Boeke, J.D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
5. Breslow, D.K., Collins, S.R., Bodenmiller, B., Aebersold, R., Simons, K., Shevchenko, A., et al. (2010) Orm family proteins mediate sphingolipid homeostasis. Nature 463: 1048-1053.
6. Brice, S.E., Alford, C.W., and Cowart, L.A. (2009) Modulation of sphingolipid metabolism by the phosphatidylinositol-4-phosphate phosphatase Sac1p through regulation of phos-phatidylinositol in Saccharomyces cerevisiae. J Biol Chem 284: 7588-7596.
7. Carman, G.M., and Henry, S.A. (1999) Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes. Prog Lipid Res 38: 361-399.
8. Catty, P., de Kerchove d'Exaerde, A., and Goffeau, A. (1997) The complete inventory of the yeast Saccharomyces cerevisiae P-type transport ATPases. FEBS Lett 409: 325-332.
9. Cerantola, V., Guillas, I., Roubaty, C., Vionnet, C., Uldry, D., Knudsen, J., and Conzelmann, A. (2009) Aureobasidin A arrests growth of yeast cells through both ceramide intoxication and deprivation of essential inositolphosphorylceramides. Mol Microbiol 71: 1523-1537.
10. Chen, C.Y., Ingram, M.F., Rosal, P.H., and Graham, T.R. (1999) Role for Drs2p, a P-type ATPase and potential aminophospholipid translocase, in yeast late Golgi function. J Cell Biol 147: 1223-1236.
11. Choi, H.S., Han, G.S., and Carman, G.M. (2010) Phosphorylation of yeast phosphatidylserine synthase by protein kinase A: identification of Ser46 and Ser47 as major sites of phosphorylation. J Biol Chem 285: 11526-11536.
12. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H., and Hieter, P. (1992) Multifunctional yeast high-copynumber shuttle vectors. Gene 110: 119-122.
13. Chung, J.H., Lester, R.L., and Dickson, R.C. (2003) Sphingolipid requirement for generation of a functional v1 component of the vacuolar ATPase. J Biol Chem 278: 28872-28881.
14. D'Angelo, G., Vicinanza, M., Di Campli, A., and De Matteis, M.A. (2008) The multiple roles of PtdIns(4)P - not just the precursor of PtdIns(4,5)P2. J Cell Sci 121: 1955-1963.
15. David, D., Sundarababu, S., and Gerst, J.E. (1998) Involvement of long chain fatty acid elongation in the trafficking of secretory vesicles in yeast. J Cell Biol 143: 1167-1182.
16. Degroote, S.,Wolthoorn, J., and van Meer, G. (2004) The cell biology of glycosphingolipids. Semin Cell Dev Biol 15: 375-387.
17. Dickson, R.C. (2008) Thematic review series: sphingolipids. New insights into sphingolipid metabolism and function in budding yeast. J Lipid Res 49: 909-921.
18. Dickson, R.C., Nagiec, E.E., Wells, G.B., Nagiec, M.M., and Lester, R.L. (1997) Synthesis of mannose-(inositol-P)2-ceramide, the major sphingolipid in Saccharomyces cerevisiae, requires the IPT1 (YDR072c) gene. J Biol Chem 272: 29620-29625.
19. Dickson, R.C., Sumanasekera, C., and Lester, R.L. (2006) Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog Lipid Res 45: 447-465.
20. Dove, S.K., Dong, K., Kobayashi, T., Williams, F.K., and Michell, R.H. (2009) Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve underPPIn endo-lysosome function. Biochem J 419: 1-13.
21. Eisenkolb, M., Zenzmaier, C., Leitner, E., and 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.
22. Endo, M., Takesako, K., Kato, I., and Yamaguchi, H. (1997) Fungicidal action of aureobasidin A, a cyclic depsipeptide antifungal antibiotic, against Saccharomyces cerevisiae. Antimicrob Agents Chemother 41: 672-676.
23. Foti, M., Audhya, A., and Emr, S.D. (2001) Sac1 lipid phosphatase and Stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology. Mol Biol Cell 12: 2396-2411.
24. Furuta, N., Fujimura-Kamada, K., Saito, K., Yamamoto, T., and Tanaka, K. (2007) Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol Biol Cell 18: 295-312.
25. Futerman, A.H., and Hannun, Y.A. (2004) The complex life of simple sphingolipids. EMBO Rep 5: 777-782.
26. Haak, D., Gable, K., Beeler, T., and Dunn, T. (1997) Hydroxylation of Saccharomyces cerevisiae ceramides requires Sur2p and Scs7p. J Biol Chem 272: 29704-29710.
27. Hama, H., Young, D.A., Radding, J.A., Ma, D., Tang, J., Stock, S.D., and Takemoto, J.Y. (2000) Requirement of sphingolipid alpha-hydroxylation for fungicidal action of syringomycin E. FEBS Lett 478: 26-28.
28. Hamamatsu, S., Shibuya, I., Takagi, M., and Ohta, A. (1994) Loss of phosphatidylserine synthesis results in aberrant solute sequestration and vacuolar morphology in Saccharomyces cerevisiae. FEBS Lett 348: 33-36.
29. Hechtberger, P., Zinser, E., Saf, R., Hummel, K., Paltauf, F., and Daum, G. (1994) Characterization, quantification and subcellular localization of inositol-containing sphingolipids of the yeast, Saccharomyces cerevisiae. Eur J Biochem 225: 641-649.
30. Herrero, A.B., Astudillo, A.M., Balboa, M.A., Cuevas, C., Balsinde, J., and Moreno, S. (2008) Levels of SCS7/FA2Hmediated fatty acid 2-hydroxylation determine the sensitivity of cells to antitumor PM02734. Cancer Res 68: 9779-9787.
31. Hua, Z., and Graham, T.R. (2003) Requirement for neo1p in retrograde transport from the Golgi complex to the endoplasmic reticulum. Mol Biol Cell 14: 4971-4983.
32. Hua, Z., Fatheddin, P., and Graham, T.R. (2002) An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol Biol Cell 13: 3162-3177.
33. Hughes, W.E., Woscholski, R., Cooke, F.T., Patrick, R.S., Dove, S.K., McDonald, N.Q., and Parker, P.J. (2000) SAC1 encodes a regulated lipid phosphoinositide phosphatase, defects in which can be suppressed by the homologous Inp52p and Inp53p phosphatases. J Biol Chem 275: 801-808.
34. Im, Y.J., Idkowiak-Baldys, J., Thevissen, K., Cammue, B.P., and Takemoto, J.Y. (2003) IPT1-independent sphingolipid biosynthesis and yeast inhibition by syringomycin E and plant defensin DmAMP1. FEMS Microbiol Lett 223: 199- 203.
35. Janitor, M., Obernauerova, M., Kohlwein, S.D., and Subik, J. (1996) The pel1 mutant of Saccharomyces cerevisiae is deficient in cardiolipin and does not survive the disruption of the CHO1 gene encoding phosphatidylserine synthase. FEMS Microbiol Lett 140: 43-47.
36. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., et al. (2004) A versatile toolbox for PCRbased tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.
37. Kihara, A., Sakuraba, H., Ikeda, M., Denpoh, A., and Igarashi, Y. (2008) Membrane topology and essential amino acid residues of Phs1, a 3-hydroxyacyl-CoA dehydratase involved in very long-chain fatty acid elongation. J Biol Chem 283: 11199-11209.
38. Klionsky, D.J., and Emr, S.D. (1989) Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J 8: 2241-2250.
39. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
40. Letts, V.A., Klig, L.S., Bae-Lee, M., Carman, G.M., and Henry, S.A. (1983) Isolation of the yeast structural gene for the membrane-associated enzyme phosphatidylserine synthase. Proc Natl Acad Sci USA 80: 7279-7283.
41. Marcusson, E.G., Horazdovsky, B.F., Cereghino, J.L., Gharakhanian, E., and Emr, S.D. (1994) The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10 gene. Cell 77: 579-586.
42. Mayinger, P., Bankaitis, V.A., and Meyer, D.I. (1995) Sac1p mediates the adenosine triphosphate transport into yeast endoplasmic reticulum that is required for protein translocation. J Cell Biol 131: 1377-1386.
43. Nagiec, M.M., Nagiec, E.E., Baltisberger, J.A., Wells, G.B., Lester, R.L., and Dickson, R.C. (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. Nakamura, H., Miura, K., Fukuda, Y., Shibuya, I., Ohta, A., and Takagi, M. (2000) Phosphatidylserine synthesis required for the maximal tryptophan transport activity in Saccharomyces cerevisiae. Biosci Biotechnol Biochem 64: 167-172.
45. Oh, C.S., Toke, D.A., Mandala, S., and Martin, C.E. (1997) ELO2 and ELO3, homologues of the Saccharomyces cerevisiae ELO1 gene, function in fatty acid elongation and are required for sphingolipid formation. J Biol Chem 272: 17376-17384.
46. Pomorski, T., Lombardi, R., Riezman, H., Devaux, P.F., van Meer, G., and Holthuis, J.C. (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol Biol Cell 14: 1240-1254.
47. Poon, P.P., Cassel, D., Spang, A., Rotman, M., Pick, E., Singer, R.A., and Johnston, G.C. (1999) Retrograde transport from the yeast Golgi is mediated by two ARF GAP proteins with overlapping function. EMBO J 18: 555-564.
48. Poon, P.P., Nothwehr, S.F., Singer, R.A., and Johnston, G.C. (2001) The Gcs1 and Age2 ArfGAP proteins provide overlapping essential function for transport from the yeast trans-Golgi network. J Cell Biol 155: 1239-1250.
49. Rivas, M.P., Kearns, B.G., Xie, Z., Guo, S., Sekar, M.C., Hosaka, K., et al. (1999) Pleiotropic alterations in lipid metabolism in yeast sac1 mutants: relationship to 'bypass Sec14p' and inositol auxotrophy. Mol Biol Cell 10: 2235-2250.
50. Robinson, J.S., Klionsky, D.J., Banta, L.M., and Emr, S.D. (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 8: 4936-4948.
51. Robinson, M., Poon, P.P., Schindler, C., Murray, L.E., Kama, R., Gabriely, G., et al. (2006) The Gcs1 Arf-GAP mediates Snc1,2 v-SNARE retrieval to the Golgi in yeast. Mol Biol Cell 17: 1845-1858.
52. Sakane, H., Yamamoto, T., and Tanaka, K. (2006) The functional relationship between the Cdc50p-Drs2p putative aminophospholipid translocase and the Arf GAP Gcs1p in vesicle formation in the retrieval pathway from yeast early endosomes to the TGN. Cell Struct Funct 31: 87-108.
53. Schorling, S., Vallee, B., Barz, W.P., Riezman, H., and 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.
54. Stearns, T., Kahn, R.A., Botstein, D., and Hoyt, M.A. (1990) ADP ribosylation factor is an essential protein in Saccharomyces cerevisiae and is encoded by two genes. Mol Cell Biol 10: 6690-6699.
55. Stock, S.D., Hama, H., Radding, J.A., Young, D.A., and Takemoto, J.Y. (2000) Syringomycin E inhibition of Saccharomyces cerevisiae: requirement for biosynthesis of sphingolipids with very-long-chain fatty acids and mannoseand phosphoinositol-containing head groups. Antimicrob Agents Chemother 44: 1174-1180.
56. Tahirovic, S., Schorr, M., and Mayinger, P. (2005) Regulation of intracellular phosphatidylinositol-4-phosphate by the Sac1 lipid phosphatase. Traffic 6: 116-130.
57. Thevissen, K., Cammue, B.P., Lemaire, K., Winderickx, J., Dickson, R.C., Lester, R.L., et al. (2000) A gene encoding a sphingolipid biosynthesis enzyme determines the sensitivity of Saccharomyces cerevisiae to an antifungal plant defensin from dahlia (Dahlia merckii). Proc Natl Acad Sci USA 97: 9531-9536.
58. Tong, A.H., and Boone, C. (2006) Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313: 171-192.
59. Uemura, S., Kihara, A., Inokuchi, J., and Igarashi, Y. (2003) Csg1p and newly identified Csh1p function in mannosylinositol phosphorylceramide synthesis by interacting with Csg2p. J Biol Chem 278: 45049-45055.
60. 2+-binding protein Csg2. J Biol Chem 282: 8613-8621.
61. Vida, T.A., and Emr, S.D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128: 779-792.
62. Whitters, E.A., Cleves, A.E., McGee, T.P., Skinner, H.B., and Bankaitis, V.A. (1993) SAC1p is an integral membrane protein that influences the cellular requirement for phospholipid transfer protein function and inositol in yeast. J Cell Biol 122: 79-94.
63. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
64. Wiradjaja, F., Ooms, L.M., Tahirovic, S., Kuhne, E., Devenish, R.J., Munn, A.L., et al. (2007) Inactivation of the phosphoinositide phosphatases Sac1p and Inp54p leads to accumulation of phosphatidylinositol 4,5-bisphosphate on vacuole membranes and vacuolar fusion defects. J Biol Chem 282: 16295-16307.
65. Yanagisawa, L.L., Marchena, J., Xie, Z., Li, X., Poon, P.P., Singer, R.A., et al. (2002) Activity of specific lipid-regulated ADP ribosylation factor-GTPase-activating proteins is required for Sec14p-dependent Golgi secretory function in yeast. Mol Biol Cell 13: 2193-2206.
66. Yoshihisa, T., and Anraku, Y. (1989) Nucleotide sequence of AMS1, the structure gene of vacuolar alpha-mannosidase of Saccharomyces cerevisiae. Biochem Biophys Res Commun 163: 908-915.
67. Zhang, C.J., Cavenagh, M.M., and Kahn, R.A. (1998) A family of Arf effectors defined as suppressors of the loss of Arf function in the yeast Saccharomyces cerevisiae. J Biol Chem 273: 19792-19796.
68. Zhang, C.J., Bowzard, J.B., Anido, A., and Kahn, R.A. (2003) Four ARF GAPs in Saccharomyces cerevisiae have both overlapping and distinct functions. Yeast 20: 315-330.
69. Zhao, C., Beeler, T., and Dunn, T. (1994) Suppressors of the Ca(2+)-sensitive yeast mutant (csg2) identify genes involved in sphingolipid biosynthesis. Cloning and characterization of SCS1, a gene required for serine palmitoyltransferase activity. J Biol Chem 269: 21480-21488.