Mannosylinositol phosphorylceramide is a major sphingolipid component and is required for proper localization of plasma-membrane proteins in Schizosaccharomyces pombe

Journal of Cell Science

Volumn 123, Issue 9, 2010, Pages 1578-1587

  Nakase, Mai ^a   Tani, Motohiro ^a   Morita, Tomotake ^b   Kitamoto, Hiroko K ^c   Kashiwazaki, Jun ^d   Nakamura, Taro ^d   Hosomi, Akira ^b   Tanaka, Naotaka ^b   Takegawa, Kaoru ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b KAGAWA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE FOR AGRO ENVIRONMENTAL SCIENCES   (Japan)

^d Osaka Prefecture University   (Japan)

Author keywords

Inositol phosphorylceramide; Lipid rafts; Mannosyltransferase; Schizosaccharomyces pombe; Sphingolipid

Indexed keywords

FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; MANNOSYLINOSITOL PHOSPHORYLCERAMIDE; NITROGEN; PROTEIN IMT1; PROTEIN IMT2; PROTEIN IMT3; SPHINGOLIPID; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL STRUCTURE; CELL VACUOLE; CONTROLLED STUDY; GENE DISRUPTION; GOLGI COMPLEX; NONHUMAN; PHENOTYPE; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES POMBE;

AMINO ACID SEQUENCE; AMINO ACID TRANSPORT SYSTEMS; CHROMATOGRAPHY, THIN LAYER; ENDOCYTOSIS; ERGOSTEROL; GENES, FUNGAL; GLYCOSPHINGOLIPIDS; INTRACELLULAR SPACE; MANNOSYLTRANSFERASES; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PROTEIN TRANSPORT; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; VACUOLES;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 77951726458     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.059139     Document Type: Article

References (72)

1. Abeijon, C., Orlean, P., Robbins, P. W. and Hirschberg, C. B. (1989). Topography of glycosylation in yeast: characterization of GDP-mannose transport and luminal guanosine diphosphatase activities in Golgi-like vesicles. Proc. Natl. Acad. Sci. USA 86, 6935-6939. (Pubitemid 19240845)
2. Alfa, C., Fantes, P., Hyams, J., McLoed, M. and Warbrick, E. (1993). Experiments with Fission Yeast: A Laboratory Course Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
3. Bagnat, M., Keranen, S., Shevchenko, A., Shevchenko, A. and Simons, K. (2000). Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. USA 97, 3254-3259. (Pubitemid 30183288)
4. Bagnat, M., Chang, A. and Simons, K. (2001). Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol. Biol. Cell 12, 4129-4138. (Pubitemid 34001097)
5. Beeler, T., Gable, K., Zhao, C. and Dunn, Y. (1994). A novel protein, CSG2p, is required for Ca2+ regulation in Saccharomyces cerevisiae. J. Biol. Chem. 269, 7279-7284. (Pubitemid 24217920)
6. Beeler, T., Fu, D., Rivera, J., Monaghan, E., Gable, K. and Dunn, T. M. (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. (Pubitemid 27416913)
7. Burd, C. G., Babst, M. and Emr, S. D. (1998). Novel pathways, membrane coats and PI kinase regulation in yeast lysosomal trafficking. Semin. Cell Dev. Biol. 9, 527-533. (Pubitemid 128353018)
8. Cowart, L. A. and Obeid, L. M. (2007). Yeast sphingolipids: recent developments in understanding biosynthesis, regulation, and function. Biochim. Biophys. Acta 1771, 421-431.
9. Dickson, R. C. (1998). Sphingolipid functions in Saccharomyces cerevisiae: comparison to mammals. Annu. Rev. Biochem. 67, 27-48. (Pubitemid 28411122)
10. 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. (Pubitemid 27508053)
11. Dickson, R. C., Sumanasekera, C. and Lester, R. L. (2006). Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid. Res. 45, 447-465. (Pubitemid 44331410)
12. Dunn, T. M., Haak, D., Monaghan, E. and Beeler, T. J. (1998). Synthesis of monohydroxylated inositolphosphorylceramide (IPC-C) in Saccharomyces cerevisiae requires Scs7p, a protein with both a cytochrome b5-like domain and a hydroxylase/desaturase domain. Yeast 14, 311-321. (Pubitemid 28138982)
13. Dupré, S. and Haguenauer-Tsapis, R. (2003). Raft partitioning of the yeast uracil permease during trafficking along the endocytic pathway. Traffic 4, 83-96. (Pubitemid 36621702)
14. Edidin, M. (2003). The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32, 257-283.
15. Feoktistova, A., Magnelli, P., Abeijon, C., Perez, P., Lester, R. L., Dickson, R. C. and Gould, K. L. (2001). Coordination between fission yeast glucan formation and growth requires a sphingolipase activity. Genetics 158, 1397-1411. (Pubitemid 32783129)
16. Gachet, Y. and Hyams, J. S. (2005). Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis. J. Cell Sci. 118, 4231-4242. (Pubitemid 41488960)
17. Gaigg, B., Toulmay, A. and Schneiter, R. (2006). Very long-chain fatty acid-containing 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. (Pubitemid 46036622)
18. Grenson, M., Hou, C. and Crabeel, M. (1970). Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. IV. Evidence for a general amino acid permease. J. Bacteriol. 103, 770-777.
19. Grimm, C., Kohli, J., Murray, J. and Maundrell, K. (1988). Genetic engineering in Schizosaccharomyces pombe: a system for gene disruption and replacement using the ura4 gene as a selectable marker. Mol. Gen. Genet. 215, 81-86. (Pubitemid 19021382)
20. Grossmann, G., Opekarova, M., Novakova, L., Stolz, J. and Tanner, W. (2006). Lipid raft-based membrane compartmentation of a plant transport protein expressed in Saccharomyces cerevisiae. Eukaryot. Cell 5, 945-953. (Pubitemid 43895024)
21. Guan, X. L., Souza, C. M., Pichler, H., Dewhurst, G., Schaad, O., Kajiwara, K., Wakabayashi, H., Ivanova, T., Castillon, G. A., Piccolis, M. et al. (2009). Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol. Biol. Cell 20, 2083-2095.
22. 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. (Pubitemid 27508064)
23. Harmouch, N., Coulon, J. and Bonaly, R. (1995). Identification of 24-methylene-24,25-dihydrolanosterol as a precursor of ergosterol in the yeasts Schizosaccharomyces pombe and Schizosaccharomyces octosporus. FEMS Microbiol. Lett. 134, 147-152.
24. Hein, C., Springael, J. Y., Volland, C., Haguenauer-Tsapis, R. and Andre, B. (1995). NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18, 77-87.
25. Holthuis, J. C., Pomorski, T., Raggers, R. J., Sprong, H. and Van Meer, G. (2001). The organizing potential of sphingolipids in intracellular membrane transport. Physiol. Rev. 81, 1689-1723. (Pubitemid 32947781)
26. Ikeda, Y., Ohashi, T., Tanaka, N. and Takegawa, K. (2009). Identification and characterization of a gene required for α1,2-mannose extension in the O-linked glycan synthesis pathway in Schizosaccharomyces pombe. FEMS Yeast Res. 9, 115-125.
27. Isshiki, T., Mochizuki, N. and Yamamoto, M. (1992). Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. Genes Dev. 6, 2455-2462. (Pubitemid 23052875)
28. +, a gene required for vacuolar biogenesis and protein sorting in Schizosaccharomyces pombe. Yeast 20, 845-855.
29. Iwaki, T., Onishi, M., Ikeuchi, M., Kita, A., Sugiura, R., Giga-Hama, Y., Fujita, Y. and Takegawa, K. (2007). Essential roles of class E Vps proteins for sorting into multivesicular bodies in Schizosaccharomyces pombe. Microbiology 153, 2753-2764.
30. Iwaki, T., Iefuji, H., Hiraga, Y., Hosomi, A., Morita, T., Giga-Hama, Y. and Takegawa, K. (2008). Multiple functions of ergosterol in the fission yeast Schizosaccharomyces pombe. Microbiology 154, 830-841. (Pubitemid 351736297)
31. Jin, H., McCaffery, J. M. and Grote, E. (2008). Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J. Cell Biol. 180, 813-826. (Pubitemid 351397780)
32. Kato, M. and Wickner, W. (2001). Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. EMBO J. 20, 4035-4040. (Pubitemid 32751820)
33. Keller, P. and Simons, K. (1997). Post-Golgi biosynthetic trafficking. J. Cell. Sci. 110, 3001-3009.
34. Kerridge, D. (1986). Mode of action of clinically important antifungal drugs. Adv. Microb. Physiol. 27, 1-72.
35. Ko, J., Chesh, S. and Fischl, A. S. (1994). Regulation of phosphatidylinositol:ceramide phosphoinositol transferase in Saccharomyces cerevisiae. J. Bacteriol. 176, 5181-5183. (Pubitemid 24253768)
36. Lauwers, E. and André, B. (2006). Association of yeast transporters with detergent-resistant membranes correlates with their cell-surface location. Traffic 7, 1045-1059.
37. Lichtenberg, D., Goni, F. M. and Heerklotz, H. (2005). Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 30, 430-436. (Pubitemid 41033238)
38. Lisman, Q., Pomorski, T., Vogelzangs, C., Urli-Stam, D., de Cocq van Delwijnen, W. and Holthuis, J. C. (2004). Protein sorting in the late Golgi of Saccharomyces cerevisiae does not require mannosylated sphingolipids. J. Biol. Chem. 279, 1020-1029. (Pubitemid 38082623)
39. Magasanik, B. and Kaiser, C. A. (2002). Nitrogen regulation in Saccharomyces cerevisiae. Gene 290, 1-18.
40. Maguy, A., Hebert, T. E. and Nattel, S. (2006). Involvement of lipid rafts and caveolae in cardiac ion channel function. Cardiovasc. Res. 69, 798-807. (Pubitemid 43227978)
41. Malinska, K., Malinsky, J., Opekarova, M. and Tanner, W. (2004). Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J. Cell. Sci. 117, 6031-6041. (Pubitemid 40123969)
42. Mellman, I. (1996). Membranes and sorting. Curr. Opin. Cell Biol. 8, 497-498.
43. Millán, J., Qaidi, M. and Alonso, M. A. (2001). Segregation of co-stimulatory components into specific T cell surface lipid rafts. Eur. J. Immunol. 31, 467-473. (Pubitemid 32166601)
44. Morita, T. and Takegawa, K. (2004). A simple and efficient procedure for transformation of Schizosaccharomyces pombe. Yeast 21, 613-617. (Pubitemid 38868180)
45. Munro, S. (2003). Lipid rafts: elusive or illusive? Cell 115, 377-388.
46. Murray, J. M. and Johnson, D. I. (2001). The Cdc42p GTPase and its regulators Nrf1p and Scd1p are involved in endocytic trafficking in the fission yeast Schizosaccharomyces pombe. J. Biol. Chem. 276, 3004-3009. (Pubitemid 37411588)
47. +-encoding syntaxin-like protein. Mol. Biol. Cell 12, 3955-3972.
48. Pelkmans, L. (2005). Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim. Biophys. Acta 1746, 295-304.
49. Prasad, T., Saini, P., Gaur, N. A., Vishwakarme, R. A., Khan, L. A., Haq, Q. M. and Prasad, R. (2005). Functional analysis of CaIPT1, a sphingolipid biosynthetic gene involved in multidrug resistance and morphogenesis of Candida albicans. Antimicrob. Agents Chemother. 49, 3442-3452. (Pubitemid 41060594)
50. Puoti, A., Desponds, C. and Conzelmann, A. (1991). Biosynthesis of mannosylinositolphosphoceramide in Saccharomyces cerevisiae is dependent on genes controlling the flow of secretory vesicles from the endoplasmic reticulum to the Golgi. J. Cell Biol. 113, 515-525. (Pubitemid 21926009)
51. Raymond, C. K., Howald-Stevenson, I., Vater, C. A. and Stevents, T. H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402. (Pubitemid 23091465)
52. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
53. Springael, J. Y. and Andre, B. (1998). Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell 9, 1253-1263. (Pubitemid 28303475)
54. Stanbrough, M., Rowen, D. W. and Magasanik, B. (1995). Role of the GATA factors Gln3p and Nil1p of Saccharomyces cerevisiae in the expression of nitrogen-regulated genes. Proc. Natl. Acad. Sci. USA 92, 9450-9454.
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 mannose- and phosphoinositol-containing head groups. Antimicrob. Agents Chemother. 44, 1174-1180. (Pubitemid 30228291)
56. Sturley, S. L. (2000). Conservation of eukaryotic sterol homeostasis: new insights from studies in budding yeast. Biochem. Biophys. Acta 1529, 155-163.
57. Tabuchi, M., Tanaka, N., Iwahara, S. and Takegawa, K. (1997). The Schizosaccharomyces pombe gms1+ gene encodes an UDP-galactose transporter homologue required for protein galactosylation. Biochem. Biophys. Res. Commun. 232, 121-125. (Pubitemid 27211932)
58. Takeda, T., Kawate, T. and Chang, F. (2004). Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast. Nat. Cell Biol. 6, 1142-1144. (Pubitemid 39468017)
59. Tanaka, N., Konomi, M., Osumi, M. and Takegawa, K. (2001). Characterization of a Schizosaccharomyces pombe mutant deficient in UDP-galactose transport activity. Yeast 18, 903-914. (Pubitemid 32677314)
60. Tanaka, N., Fujita, Y., Suzuki, S., Morishita, M., Giga-Hama, Y., Shimoda, C. and Takegawa, K. (2005). Charaterization of O-mannosyltransferase family in Schizosaccharomyces pombe. Biochem. Biophys. Res. Commun. 330, 813-820. (Pubitemid 40462159)
61. Tanida, I., Takita, Y., Hasegawa, A., Ohya, Y. and Anraku, Y. (1996). Yeast Cls2p/Csg2p localized on the endoplasmic reticulum membrane regulates a non-exchangeable intracellular Ca2+ pool cooperatively with calcineurin. FEBS Lett. 379, 38-42. (Pubitemid 126334520)
62. 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. (Pubitemid 37432636)
63. 2+-binding protein Csg2. J. Biol. Chem. 282, 8613-8621.
64. Umebayashi, K. and Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J. Cell Biol. 161, 1117-1131. (Pubitemid 36870173)
65. Van Meer, G. and Simons, K. (1988). Lipid polarity and sorting in epithelial cells. J. Cell Biochem. 36, 51-58.
66. 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.
67. Wachtler, V. and Balasubramanian, M. K. (2006). Yeast lipid rafts? - an emerging view. Trends Cell Biol. 16, 1-4. (Pubitemid 43077088)
68. Wachtler, V., Pajagopalan, S. and Balasubramanian, M. K. (2003). Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J. Cell. Sci. 116, 867-874. (Pubitemid 36367636)
69. Wiggins, C. A. and Munro, S. (1998). Activity of the yeast MNN1 α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl. Acad. Sci. USA 95, 7945-7950.
70. Wood, V., Gwilliam, R., Rajandream, M. A., Lyne, M., Lyne, R., Stewart, A., Sgouros, J., Peat, N., Hayles, J., Baker, S. et al. (2002). The genome sequence of Schizosaccharomyces pombe. Nature 415, 871-880.
71. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze. C. and London, E. (2001). 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. 276, 33540-33546. (Pubitemid 37384566)
72. Zink, S., Methlgarten, C., Kitamoto, H. K., Nagase, J., Jablonowski, D., Dickson, R. C., Stark, M. J. and Schaffrath, R. (2005). Mannosyl- diinositolphospho-ceramide, the major yeast plasma membrane sphingolipid, governs toxicity of Kluyveromyces lactis zymocin. Eukaryot. Cell 4, 879-889. (Pubitemid 40697752)