PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity

Microbiology

Volumn 150, Issue 12, 2004, Pages 4157-4170

  Pardo, Mercedes ^a,b   Monteoliva, Lucía ^a   Vázquez, Paloma ^a   Martínez, Raquel ^a   Molero, Gloria ^a   Nombela, César ^a   Gil, Concha ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; GLYCOSYLATED PROTEIN; MANNOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CELL ULTRASTRUCTURE; CELL WALL; CONTROLLED STUDY; CYTOPLASM; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTOPLAST; SEQUENCE HOMOLOGY; YEAST;

CELL WALL; GENE EXPRESSION REGULATION, FUNGAL; GLYCOSYLPHOSPHATIDYLINOSITOLS; MEMBRANE PROTEINS; MUTATION; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 6444229572     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.26924-0     Document Type: Article

References (77)

1. Ausubel, F. M., Kingston, R. E., Brent, R., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1993). Current Protocols in Molecular Biology. New York: Greene Publishing Associates and Wiley Interscience.
2. Ballou, C. E. (1990). Isolation, characterization, and properties of Saccharomyces cerevisiae mnn mutants with nonconditional protein glycosylation defects. Methods Enzymol 185, 440-470.
3. Ballou, L., Hitzeman, R. A., Lewis, M. S. & Ballou, C. E. (1991). Vanadate-resistant yeast mutants are defective in protein glycosylation. Proc Natl Acad Sci U S A 88, 3209-3212.
4. Benachour, A., Sipos, G., Flury, I., Reggiori, F., Canivenc-Gansel, E., Vionnet, C., Conzelmann, A. & Benghezal, M. (1999). Deletion of GPI7, a yeast gene required for addition of a side chain to the glycosylphosphatidylinositol (GPI) core structure, affects GPI protein transport, remodeling, and cell wall integrity. J Biol Chem 274, 15251-15261.
5. Bidlingmaier, S. & Snyder, M. (2002). Large-scale identification of genes important for apical growth in Saccharomyces cerevisiae by directed allele replacement technology (DART) screening. Funct Integr Genomics 1, 345-356.
6. Bordier, C. (1981). Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 256, 1604-1607.
7. Bruneau, J. M., Magnin, T., Tagat, E., Legrand, R., Bernard, M., Diaquin, M., Fudali, C. & Latgé, J.-P. (2001 . Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22, 2812-2823.
8. Bussey, H. (1991). K1 killer toxin, a pore-forming protein from yeast. Mol Microbiol 5, 2339-2343.
9. Cabib, E., Roh, D.-H., Schmidt, M., Crotti, L. B. & Varma, A. (2001). The yeast cell wall and septum as paradigms of cell growth and morphogenesis. J Biol Chem 276, 19679-19682.
10. Caro, L. H. P., Tettelin, H., Vossen, J. H., Ram, A. F. J., Van den Ende, H. & Klis, F. M. (1997). In silicio identification of glycosylphosphatidylinositol-anchored plasma membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13, 1477-1489.
11. Chavan, M., Suzuki, T., Rekowicz, M. & Lennarz, W. (2003). Genetic, biochemical and morphological evidence for the involvement of N-glycosylation in biosynthesis of the cell wall β1,6-glucan of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 100, 15381-15386.
12. Cid, V. J., Durán, A., del Rey, F., Snyder, M. P., Nombela, C. & Sánchez, M. (1995). Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. Microbiol Rev 59 345-386.
13. Colman-Lerner, A., Chin, T. E. & Brent, R. (2001). Yeast cbk1 and mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107, 739-750.
14. Conde, R., Pablo, G., Cueva, R. & Larriba, G. (2003). Screening for new yeast mutants affected in mannosylphosphorylation of cell wall mannoproteins. Yeast 20, 1189-1211.
15. Conzelmann, A., Spiazzi, A., Hyman, R. & Bron, C. (1986). Anchoring of membrane proteins via phosphatidylinositol is deficient in two classes of Thy-1 negative mutant lymphoma cells. EMBO J 5 3291-3296.
16. Conzelmann, A., Riezman, H., Desponds, C. & Bron, C. (1988). A major 125-kd membrane glycoprotein of Saccharomyces cerevisiae is attached to the lipid bilayer through an inositol-containing phospholipid. EMBO J 7, 2233-2240.
17. Dean, N. (1995). Yeast glycosylation mutants are sensitive to aminoglycosides. Proc Natl Acad Sci U S A 92, 1287-1291.
18. de Groot, P. W., Ruíz, C., Vázquez de Aldana, C. R. & 14 other authors (2001). A genomic approach for the identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp Funct Genomics 2 1-19.
19. de Nobel, H., Ruiz, C., Martín, H., Morris, W., Brul, S., Molina, M. & Klis, F. M. (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.
20. de Sampaïo, G., Bourdineaud, J. P. & Lauquin, G. J. M. (1999). A constitutive role for GPI anchors in Saccharomyces cerevisiae: cell wall targeting. Mol Microbiol 34, 247-256.
21. Ecker, M., Hagen, I., Sestak, S., Strahl-Bolsinger, S., Mrsǎ, V. & Tanner, W. (2003). News from the covalently linked cell wall protein Ccw5/Pir4. Poster at II International Conference on Molecular Mechanisms of Fungal Cell Wall Biogenesis. Salamanca, Spain.
22. Garí, E., Piedrafita, L., Aldea, M. & Herrero, E. (1997). A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 13, 837-848.
23. Garrett, T. P., McKern, N. M., Lou, M., Frenkel, M. J., Bentley, J. D., Lovrecz, G. O., Elleman, T. C., Cosgrove, L. J. & Ward, C. W. (1998). Crystal structure of the first three domains of the type-1 insulin-like growth factor receptor. Nature 394, 395-399.
24. +-ATPase. Mol Cell Biol 15, 4103-4114.
25. Hamada, K, Fukuchi, S., Arisawa, M., Baba, M. & Kitada, K. (1998a). Screening for glycosylphosphatidylinositol (GPI)-dependent cell wall proteins in Saccharomyces cerevisiae. Mol Gen Genet 258, 53-59.
26. Hamada, K., Terashima, H., Arisawa, M. & Kitada, K. (1998b). Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol-associated proteins into the cell wall of Saccharomyces cerevisiae. J Biol Chem 273, 26946-26953.
27. Hamada, K., Terashima, H., Arisawa, M., Yabuki, N. & Kitada, K. (1999). Amino acid residues in the ω-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J Bacteriol 181 3886-3889.
28. Hutchins, K. & Bussey, H. (1983). Cell wall receptor for yeast killer toxin: involvement of (1→6)-beta-D-glucan. J Bacteriol 154, 161-169.
29. Jung, U. S. & Levin, D. E. (1999). Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol Microbiol 34, 1049-1057.
30. Kanik-Ennulat, C., Montalvo, E. & Neff, N. (1995). Sodium orthovanadate-resistant mutants of Saccharomyces cerevisiae show defects in Golgi-mediated protein glycosylation, sporulation and detergent resistance. Genetics 140, 933-943.
31. Kapteyn, J. C., Montijn, R. C., Vink, E., de la Cruz, J., Llobell, A., Douwes, J. E., Shimoi, H., Lipke, P. N. & Klis, F. M. (1996). Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. Glycobiology 6, 337-345.
32. Kapteyn, J. C., Ram, A. F., Groos, E. M., Kollar, R., Montijn, R. C., Van den Ende, H., Llobell, A., Cabib, E. & Klis, F. M. (1997). Altered extent of cross-linking of β1,6-glucosylated mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall β1,3-glucan content. J Bacteriol 179, 6279-6284.
33. Kapteyn, J. C., Van den Ende, H. & Klis, F. M. (1999a). The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta 1426, 373-383.
34. Kapteyn, J. C., van Egmond, P., Sievi, E., Van den Ende, H., Makarow, M. & Klis, F. M. (1999b). The contribution of the O glycosylated protein Pir2p/Hsp150 to the construction of the yeast cell wall in wild-type cells and β1,6-glucan-deficient mutants. Mol Microbiol 31, 1835-1844.
35. Klis, F. M. (1994). Review: cell wall assembly in yeast. Yeast 10, 851-869.
36. Klis, F. M., Ram, A. F. J., Montijn, R. C., Kapteyn, J. C., Caro, L. H. P., Vossen, J. H., Van Berkel, M. A. A., Brekelmans, S. S. C. & Van den Ende, H. (1998). Posttranslational modifications of secretory proteins. In Yeast Gene Analysis, vol. 26, pp. 223-238. Edited by A. J. P. Brown & M. F. Tuite. Amsterdam: Academic Press.
37. Klis, F. M., Mol, P., Hellingwerf, K & Brul, S. (2002). Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26, 239-256.
38. Kollár, R., Petrakova, E., Ashwell, G., Robbins, P. W. & Cabib, E. (1995). Architecture of the yeast cell wall. The linkage between chitin and β(1→3)-glucan. J Biol Chem 270, 1170-1178.
39. Kollár, R., Reinhold, B. B., Petrakova, E., Yeh, H. J., Ashwell, G., Drgonova, J., Kapteyn, J. C., Klis, F. M. & Cabib, E. (1997). Architecture of the yeast cell wall. β(1→6)-glucan interconnects mannoprotein, β(1→3)-glucan, and chitin. J Biol Chem 272, 17762-17775.
40. Kopecka, M. & Gabriel, M. (1992). The influence of congo red on the cell wall and (1→3)-beta-D-glucan microfibril biogenesis in Saccharomyces cerevisiae. Arch Microbiol 158, 115-126.
41. Kumar, A., Cheung, K. H., Ross-Macdonald, P., Coelho, P. S., Miller, P. & Snyder, M. (2000). TRIPLES: a database of gene function in Saccharomyces cerevisiae. Nucleic Acids Res 28, 81-84.
42. Lagorce, A., Hauser, N. C., Labourdette, D., Rodriguez, C., Martin-Yken, H., Arroyo, J., Hoheisel, J. D. & Francois, J. (2003). Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J Biol Chem 278, 20345-20357.
43. Lee, K. S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., Matsumoto, K. & Levin, D. E. (1993). A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol Cell Biol 13, 3067-3075.
44. Lipke, P. N. & Ovalle, R. (1998). Cell wall architecture in yeast: new structure and new challenges. J Bacteriol 180, 3735-3740.
45. Lussier, M., White, A. M., Sheraton, J. & 17 other authors (1997). Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147, 435-450.
46. Martín, H., Arroyo, J., Sánchez, M., Molina, M. & Nombela, C. (1993). Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37 degrees C. Mol Gen Genet 241, 177-184.
47. Martín, H., Rodríguez-Pachón, J. M., Ruí z, C., Nombela, C. & Molina, M. (2000). Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J Biol Chem 275, 1511-1519.
48. Miret, J. J., Solari, A. J., Barderi, P. A. & Goldemberg, S. H. (1992). Polyamines and cell wall organization in Saccharomyces cerevisiae. Yeast 8, 1033-1041.
49. Molina, M., Gil, C., Pla, J., Arroyo, J. & Nombela, C. (2000). Protein localisation approaches for understanding yeast cell wall biogenesis. Microsc Res Tech 51, 601-612.
50. Monteoliva, L., Matas, M. L., Gil, C., Nombela, C. & Pla, J. (2002). Large-scale identification of putative exported proteins in Candida albicans by genetic selection. Eukaryot Cell 1, 514-525.
51. Montijn, R. C., van Rinsum, J., van Schagen, F. A. & Klis, F. M. (1994). Glucomannoproteins in the cell wall of Saccharomyces cerevisiae contain a novel type of carbohydrate side chain. J Biol Chem 269, 19338-19342.
52. Mrsǎ V., Seidl, T., Gentzsh, M. & Tanner, W. (1997). Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13, 1145-1154.
53. Orlean, P. (1997). Biogenesis of yeast cell wall and surface components. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Cell Cycle and Biology, pp. 229-362. Edited by J. R. Pringle, J. R. Broach & E. W. Jones. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
54. Pardo, M., Monteoliva, L., Pla, J., Sanchez, M., Gil, C. & Nombela, C. (1999). Two-dimensional analysis of proteins secreted by Saccharomyces cerevisiae regenerating protoplasts: a novel approach to study the cell wall. Yeast 15, 459-472.
55. Pardo, M., Ward, M., Bains, S., Molina, M., Blackstock W., Gil, C. & Nombela, C. (2000). A proteomic approach for the study of Saccharomyces cerevisiae cell wall biogenesis. Electrophoresis 21, 3396-3410.
56. Percival-Smith, A. & Segall, I. (1987). Increased copy number of the 5′ end of the SPS2 gene inhibits sporulation of Saccharomyces cerevisiae. Mol Cell Biol 7, 2484-2490.
57. Pringle, J. R., Adams, A. E. M., Drubin, D. G. & Haarer, B. K. (1991). Immunofluorescence methods for yeast. In Guide to Yeast Genetics and Molecular Biology, pp. 565-602. Edited by C. Guthrie & G. R. Fink. London: Academic Press.
58. Ram, A. F., Kapteyn, J. C., Montijn, R. C., Caro, L. H., Douwes, J. E., Baginsky, W., Mazur, P., Van den Ende, H. & Klis, F. M. (1998). Loss of the plasma membrane-bound protein Gas1p in Saccharomyces cerevisiae results in the release of β 1,3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity. J Bacteriol 180, 1418-1424.
59. Reddy, V. A., Johnson, R. S., Biemann, K., Williams, R. S., Ziegler, F. D., Trimble, R. B. & Maley, F. (1988). Characterization of the glycosylation sites in yeast external invertase. I. N-linked oligosaccharide content of the individual sequons. J Biol Chem 263, 6978-6985.
60. Richard, M., de Groot, P., Courtin, O., Poulain, D., Klis, F. & Gaillardin, C. (2002). GPI7 affects cell wall protein anchorage in Saccharomyces cerevisiae and Candida albicans. Microbiology 148, 2125-2133.
61. Rodríguez-Peña, J. M., Cid, V. J., Arroyo, J. & Nombela, C. (2000). A novel family of cell wall-related proteins regulated differently during the yeast life cycle. Mol Cell Biol 20, 3245-3255.
62. Roemer, T., Paravicini, G., Payton, M. A. & Bussey, H. (1994). Characterization of the yeast (1-6)-beta-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly. J Cell Biol 127 567-579.
63. Roncero, C. & Durán, A. (1985). Effect of Calcofluor White and Congo Red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J Bacteriol 163, 1180-1185.
64. Ross-Macdonald, P., Coelho, P. S., Roemer, T. & 15 other authors (1999). Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402, 413-418.
65. Ruíz, C., Cid, V. J., Lussier, M., Molina, M. & Nombela, C. (1999). A large-scale sonication assay for cell wall mutant analysis in yeast. Yeast 15, 1001-1008.
66. Russo, P., Kalkkinen, N., Sareneva, H., Paakkola, J. & Makarow, M. (1992). A heat shock gene from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc Natl Acad Sci U S A 89, 3671-3675.
67. Shahinian, S. & Bussey, H. (2000). β-1,6-Glucan synthesis in Saccharomyces cerevisiae. Mol Microbiol 35, 477-489.
68. Souciet, J., Aigle, M., Artiguenave, F. & 22 other authors (2000). Genomic exploration of the hemiascomycetous yeasts: 1. A set of yeast species for molecular evolution studies. FEBS Lett 487 3-12.
69. Spellman, P. T., Sherlock G., Zhang, M. Q., Iyer, V. R., Anders, K, Eisen, M. B., Brown, P. O., Botstein, D. & Futcher, B. (1998). Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9, 3273-3297.
70. Terashima, H., Yabuki, N., Fukuchi, S., Hamada, K., Arisawa, M. & Kitada, K. (1999). Yeast genes induced by defects of the glucan biosynthesis. Curr Genet 35, 444.
71. Terashima, H., Hamada, K. & Kitada, K. (2003). The localization change of Ybr078w/Ecm33, a yeast GPI-associated protein, from the plasma membrane to the cell wall, affecting the cellular function. FEMS Microbiol Lett 218, 175-180.
72. Toh-E, A. & Oguchi, T. (2002). Genetic characterization of genes encoding enzymes catalyzing addition of phospho-ethanolamine to the glycosylphosphatidylinositol anchor in Saccharomyces cerevisiae. Genes Genet Syst 77, 309-322.
73. Tong, A. H., Lesage, G., Bader, G. D. & 47 other authors (2004). Global mapping of the yeast genetic interaction network. Science 303, 808-813.
74. Tougan, T., Chiba, Y., Kakihara, Y., Hirata, A. & Nojima, H. (2002). Meu10 is required for spore wall maturation in Schizosaccharomyces pombe. Genes Cells 7, 217-231.
75. Turchini, A., Ferrario, L. & Popolo, L. (2000). Increase of external osmolarity reduces morphogenetic defects and accumulation of chitin in a gas1 mutant of Saccharomyces cerevisiae. J Bacteriol 182, 1167-1171.
76. Wach, A., Brachat A., Pohlmann, R. & Philippsen, P. (1994). New heterologous modules for classical or PCR-band gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
77. Winston, F., Dollard, C. & Ricupero-Hovasse, S. L. (1995). Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11, 53-55.